diff --git a/packages/client/src/components/app/forms/RelationshipField.svelte b/packages/client/src/components/app/forms/RelationshipField.svelte
index 54171309de..c40041c7d6 100644
--- a/packages/client/src/components/app/forms/RelationshipField.svelte
+++ b/packages/client/src/components/app/forms/RelationshipField.svelte
@@ -1,18 +1,15 @@
 <script lang="ts">
   import { CoreSelect, CoreMultiselect } from "@budibase/bbui"
-  import { FieldType } from "@budibase/types"
+  import { FieldType, InternalTable } from "@budibase/types"
   import { fetchData, Utils } from "@budibase/frontend-core"
   import { getContext } from "svelte"
   import Field from "./Field.svelte"
   import type {
     SearchFilter,
     RelationshipFieldMetadata,
-    Table,
     Row,
   } from "@budibase/types"
 
-  const { API } = getContext("sdk")
-
   export let field: string | undefined = undefined
   export let label: string | undefined = undefined
   export let placeholder: any = undefined
@@ -20,10 +17,10 @@
   export let readonly: boolean = false
   export let validation: any
   export let autocomplete: boolean = true
-  export let defaultValue: string | undefined = undefined
+  export let defaultValue: string | string[] | undefined = undefined
   export let onChange: any
   export let filter: SearchFilter[]
-  export let datasourceType: "table" | "user" | "groupUser" = "table"
+  export let datasourceType: "table" | "user" = "table"
   export let primaryDisplay: string | undefined = undefined
   export let span: number | undefined = undefined
   export let helpText: string | undefined = undefined
@@ -32,191 +29,305 @@
     | FieldType.BB_REFERENCE
     | FieldType.BB_REFERENCE_SINGLE = FieldType.LINK
 
-  type RelationshipValue = { _id: string; [key: string]: any }
-  type OptionObj = Record<string, RelationshipValue>
-  type OptionsObjType = Record<string, OptionObj>
+  type BasicRelatedRow = { _id: string; primaryDisplay: string }
+  type OptionsMap = Record<string, BasicRelatedRow>
 
+  const { API } = getContext("sdk")
+
+  // Field state
   let fieldState: any
   let fieldApi: any
   let fieldSchema: RelationshipFieldMetadata | undefined
-  let tableDefinition: Table | null | undefined
-  let searchTerm: any
-  let open: boolean
-  let selectedValue: string[] | string
 
-  // need a cast version of this for reactivity, components below aren't typed
-  $: castSelectedValue = selectedValue as any
+  // Local UI state
+  let searchTerm: any
+  let open: boolean = false
+
+  // Options state
+  let options: BasicRelatedRow[] = []
+  let optionsMap: OptionsMap = {}
+  let loadingMissingOptions: boolean = false
+
+  // Determine if we can select multiple rows or not
   $: multiselect =
     [FieldType.LINK, FieldType.BB_REFERENCE].includes(type) &&
     fieldSchema?.relationshipType !== "one-to-many"
-  $: linkedTableId = fieldSchema?.tableId!
-  $: fetch = fetchData({
-    API,
-    datasource: {
-      // typing here doesn't seem correct - we have the correct datasourceType options
-      // but when we configure the fetchData, it seems to think only "table" is valid
-      type: datasourceType as any,
-      tableId: linkedTableId,
-    },
-    options: {
-      filter,
-      limit: 100,
-    },
-  })
 
-  $: tableDefinition = $fetch.definition
-  $: selectedValue = multiselect
-    ? flatten(fieldState?.value) ?? []
-    : flatten(fieldState?.value)?.[0]
-  $: component = multiselect ? CoreMultiselect : CoreSelect
-  $: primaryDisplay = primaryDisplay || tableDefinition?.primaryDisplay
+  // Get the proper string representation of the value
+  $: realValue = fieldState?.value
+  $: selectedValue = parseSelectedValue(realValue, multiselect)
+  $: selectedIDs = getSelectedIDs(selectedValue)
 
-  let optionsObj: OptionsObjType = {}
-  const debouncedFetchRows = Utils.debounce(fetchRows, 250)
+  // If writable, we use a fetch to load options
+  $: linkedTableId = fieldSchema?.tableId
+  $: writable = !disabled && !readonly
+  $: fetch = createFetch(writable, datasourceType, filter, linkedTableId)
 
-  $: {
-    if (primaryDisplay && fieldState && !optionsObj) {
-      // Persist the initial values as options, allowing them to be present in the dropdown,
-      // even if they are not in the inital fetch results
-      let valueAsSafeArray = fieldState.value || []
-      if (!Array.isArray(valueAsSafeArray)) {
-        valueAsSafeArray = [fieldState.value]
-      }
-      optionsObj = valueAsSafeArray.reduce(
-        (
-          accumulator: OptionObj,
-          value: { _id: string; primaryDisplay: any }
-        ) => {
-          // fieldState has to be an array of strings to be valid for an update
-          // therefore we cannot guarantee value will be an object
-          // https://linear.app/budibase/issue/BUDI-7577/refactor-the-relationshipfield-component-to-have-better-support-for
-          if (!value._id) {
-            return accumulator
+  // Attempt to determine the primary display field to use
+  $: tableDefinition = $fetch?.definition
+  $: primaryDisplayField = primaryDisplay || tableDefinition?.primaryDisplay
+
+  // Build our options map
+  $: rows = $fetch?.rows || []
+  $: processOptions(realValue, rows, primaryDisplayField)
+
+  // If we ever have a value selected for which we don't have an option, we must
+  // fetch those rows to ensure we can render them as options
+  $: missingIDs = selectedIDs.filter(id => !optionsMap[id])
+  $: loadMissingOptions(missingIDs, linkedTableId, primaryDisplayField)
+
+  // Convert our options map into an array for display
+  $: updateOptions(optionsMap)
+  $: !open && sortOptions()
+
+  // Search for new options when search term changes
+  $: debouncedSearchOptions(searchTerm || "", primaryDisplayField)
+
+  // Ensure backwards compatibility
+  $: enrichedDefaultValue = enrichDefaultValue(defaultValue)
+
+  // We need to cast value to pass it down, as those components aren't typed
+  $: emptyValue = multiselect ? [] : null
+  $: displayValue = missingIDs.length ? emptyValue : (selectedValue as any)
+
+  // Ensures that we flatten any objects so that only the IDs of the selected
+  // rows are passed down. Not sure how this can be an object to begin with?
+  const parseSelectedValue = (
+    value: any,
+    multiselect: boolean
+  ): undefined | string | string[] => {
+    return multiselect ? flatten(value) : flatten(value)[0]
+  }
+
+  // Where applicable, creates the fetch instance to load row options
+  const createFetch = (
+    writable: boolean,
+    dsType: typeof datasourceType,
+    filter: SearchFilter[],
+    linkedTableId?: string
+  ) => {
+    if (!linkedTableId) {
+      return undefined
+    }
+    const datasource =
+      datasourceType === "table"
+        ? {
+            type: datasourceType,
+            tableId: fieldSchema?.tableId!,
           }
-          accumulator[value._id] = {
-            _id: value._id,
-            [primaryDisplay]: value.primaryDisplay,
+        : {
+            type: datasourceType,
+            tableId: InternalTable.USER_METADATA,
           }
-          return accumulator
-        },
-        {}
-      )
-    }
-  }
-
-  $: enrichedOptions = enrichOptions(optionsObj, $fetch.rows)
-  const enrichOptions = (optionsObj: OptionsObjType, fetchResults: Row[]) => {
-    const result = (fetchResults || [])?.reduce((accumulator, row) => {
-      if (!accumulator[row._id!]) {
-        accumulator[row._id!] = row
-      }
-      return accumulator
-    }, optionsObj || {})
-
-    return Object.values(result)
-  }
-  $: {
-    // We don't want to reorder while the dropdown is open, to avoid UX jumps
-    if (!open && primaryDisplay) {
-      enrichedOptions = enrichedOptions.sort((a: OptionObj, b: OptionObj) => {
-        const selectedValues = flatten(fieldState?.value) || []
-
-        const aIsSelected = selectedValues.find(
-          (v: RelationshipValue) => v === a._id
-        )
-        const bIsSelected = selectedValues.find(
-          (v: RelationshipValue) => v === b._id
-        )
-        if (aIsSelected && !bIsSelected) {
-          return -1
-        } else if (!aIsSelected && bIsSelected) {
-          return 1
-        }
-
-        return (a[primaryDisplay] > b[primaryDisplay]) as unknown as number
-      })
-    }
-  }
-
-  $: {
-    if (filter || defaultValue) {
-      forceFetchRows()
-    }
-  }
-  $: debouncedFetchRows(searchTerm, primaryDisplay, defaultValue)
-
-  const forceFetchRows = async () => {
-    // if the filter has changed, then we need to reset the options, clear the selection, and re-fetch
-    optionsObj = {}
-    fieldApi?.setValue([])
-    selectedValue = []
-    debouncedFetchRows(searchTerm, primaryDisplay, defaultValue)
-  }
-  async function fetchRows(
-    searchTerm: any,
-    primaryDisplay: string,
-    defaultVal: string | string[]
-  ) {
-    const allRowsFetched =
-      $fetch.loaded &&
-      !Object.keys($fetch.query?.string || {}).length &&
-      !$fetch.hasNextPage
-    // Don't request until we have the primary display or default value has been fetched
-    if (allRowsFetched || !primaryDisplay) {
-      return
-    }
-    // must be an array
-    const defaultValArray: string[] = !defaultVal
-      ? []
-      : !Array.isArray(defaultVal)
-      ? defaultVal.split(",")
-      : defaultVal
-
-    if (
-      defaultVal &&
-      optionsObj &&
-      defaultValArray.some(val => !optionsObj[val])
-    ) {
-      await fetch.update({
-        query: { oneOf: { _id: defaultValArray } },
-      })
-    }
-
-    if (
-      (Array.isArray(selectedValue) &&
-        selectedValue.some(val => !optionsObj[val])) ||
-      (selectedValue && !optionsObj[selectedValue as string])
-    ) {
-      await fetch.update({
-        query: {
-          oneOf: {
-            _id: Array.isArray(selectedValue) ? selectedValue : [selectedValue],
-          },
-        },
-      })
-    }
-
-    // Ensure we match all filters, rather than any
-    // @ts-expect-error this doesn't fit types, but don't want to change it yet
-    const baseFilter: any = (filter || []).filter(x => x.operator !== "allOr")
-    await fetch.update({
-      filter: [
-        ...baseFilter,
-        {
-          // Use a big numeric prefix to avoid clashing with an existing filter
-          field: `999:${primaryDisplay}`,
-          operator: "string",
-          value: searchTerm,
-        },
-      ],
+    return fetchData({
+      API,
+      datasource,
+      options: {
+        filter,
+        limit: writable ? 100 : 1,
+      },
     })
   }
 
-  const flatten = (values: any | any[]) => {
+  // Small helper to represent the selected value as an array
+  const getSelectedIDs = (
+    selectedValue: undefined | string | string[]
+  ): string[] => {
+    if (!selectedValue) {
+      return []
+    }
+    return Array.isArray(selectedValue) ? selectedValue : [selectedValue]
+  }
+
+  // Builds a map of all available options, in a consistent structure
+  const processOptions = (
+    realValue: any | any[],
+    rows: Row[],
+    primaryDisplay?: string
+  ) => {
+    // First ensure that all options included in the value are present as valid
+    // options. These can be basic related row shapes which already include
+    // a value for primary display
+    if (realValue) {
+      const valueArray = Array.isArray(realValue) ? realValue : [realValue]
+      for (let val of valueArray) {
+        const option = parseOption(val, primaryDisplay)
+        if (option) {
+          optionsMap[option._id] = option
+        }
+      }
+    }
+
+    // Process all rows loaded from our fetch
+    for (let row of rows) {
+      const option = parseOption(row, primaryDisplay)
+      if (option) {
+        optionsMap[option._id] = option
+      }
+    }
+
+    // Reassign to trigger reactivity
+    optionsMap = optionsMap
+  }
+
+  // Parses a row-like structure into a properly shaped option
+  const parseOption = (
+    option: any | BasicRelatedRow | Row,
+    primaryDisplay?: string
+  ): BasicRelatedRow | null => {
+    if (!option || typeof option !== "object" || !option?._id) {
+      return null
+    }
+    // If this is a basic related row shape (_id and PD only) then just use
+    // that
+    if (Object.keys(option).length === 2 && "primaryDisplay" in option) {
+      return {
+        _id: option._id,
+        primaryDisplay: ensureString(option.primaryDisplay),
+      }
+    }
+    // Otherwise use the primary display field specified
+    if (primaryDisplay) {
+      return {
+        _id: option._id,
+        primaryDisplay: ensureString(
+          option[primaryDisplay as keyof typeof option]
+        ),
+      }
+    } else {
+      return {
+        _id: option._id,
+        primaryDisplay: option._id,
+      }
+    }
+  }
+
+  // Loads any rows which are selected and aren't present in the currently
+  // available option set. This is typically only IDs specified as default
+  // values.
+  const loadMissingOptions = async (
+    missingIDs: string[],
+    linkedTableId?: string,
+    primaryDisplay?: string
+  ) => {
+    if (
+      loadingMissingOptions ||
+      !missingIDs.length ||
+      !linkedTableId ||
+      !primaryDisplay
+    ) {
+      return
+    }
+    loadingMissingOptions = true
+    try {
+      const res = await API.searchTable(linkedTableId, {
+        query: {
+          oneOf: {
+            _id: missingIDs,
+          },
+        },
+      })
+      for (let row of res.rows) {
+        const option = parseOption(row, primaryDisplay)
+        if (option) {
+          optionsMap[option._id] = option
+        }
+      }
+
+      // Reassign to trigger reactivity
+      optionsMap = optionsMap
+      updateOptions(optionsMap)
+    } catch (error) {
+      console.error("Error loading missing row IDs", error)
+    } finally {
+      // Ensure we have some sort of option for all IDs
+      for (let id of missingIDs) {
+        if (!optionsMap[id]) {
+          optionsMap[id] = {
+            _id: id,
+            primaryDisplay: id,
+          }
+        }
+      }
+      loadingMissingOptions = false
+    }
+  }
+
+  // Updates the options list to reflect the currently available options
+  const updateOptions = (optionsMap: OptionsMap) => {
+    let newOptions = Object.values(optionsMap)
+
+    // Only override options if the quantity of options changes
+    if (newOptions.length !== options.length) {
+      options = newOptions
+      sortOptions()
+    }
+  }
+
+  // Sorts the options list by selected state, then by primary display
+  const sortOptions = () => {
+    // Create a quick lookup map so we can test whether options are selected
+    const selectedMap: Record<string, boolean> = selectedIDs.reduce(
+      (map, id) => ({ ...map, [id]: true }),
+      {}
+    )
+    options.sort((a, b) => {
+      const aSelected = !!selectedMap[a._id]
+      const bSelected = !!selectedMap[b._id]
+      if (aSelected === bSelected) {
+        return a.primaryDisplay < b.primaryDisplay ? -1 : 1
+      } else {
+        return aSelected ? -1 : 1
+      }
+    })
+  }
+
+  // Util to ensure a value is stringified
+  const ensureString = (val: any): string => {
+    return typeof val === "string" ? val : JSON.stringify(val)
+  }
+
+  // We previously included logic to manually process default value, which
+  // should not be done as it is handled by the core form logic.
+  // This logic included handling a comma separated list of IDs, so for
+  // backwards compatibility we must now unfortunately continue to handle that
+  // at this level.
+  const enrichDefaultValue = (val: any) => {
+    if (!val || typeof val !== "string") {
+      return val
+    }
+    return val.includes(",") ? val.split(",") : val
+  }
+
+  // Searches for new options matching the given term
+  async function searchOptions(searchTerm: string, primaryDisplay?: string) {
+    if (!primaryDisplay) {
+      return
+    }
+
+    // Ensure we match all filters, rather than any
+    let newFilter: any = filter
+    if (searchTerm) {
+      // @ts-expect-error this doesn't fit types, but don't want to change it yet
+      newFilter = (newFilter || []).filter(x => x.operator !== "allOr")
+      newFilter.push({
+        // Use a big numeric prefix to avoid clashing with an existing filter
+        field: `999:${primaryDisplay}`,
+        operator: "string",
+        value: searchTerm,
+      })
+    }
+    await fetch?.update({
+      filter: newFilter,
+    })
+  }
+  const debouncedSearchOptions = Utils.debounce(searchOptions, 250)
+
+  // Flattens an array of row-like objects into a simple array of row IDs
+  const flatten = (values: any | any[]): string[] => {
     if (!values) {
       return []
     }
-
     if (!Array.isArray(values)) {
       values = [values]
     }
@@ -226,16 +337,11 @@
     return values
   }
 
-  const getDisplayName = (row: Row) => {
-    return row?.[primaryDisplay!] || "-"
-  }
-
   const handleChange = (e: any) => {
     let value = e.detail
     if (!multiselect) {
       value = value == null ? [] : [value]
     }
-
     if (
       type === FieldType.BB_REFERENCE_SINGLE &&
       value &&
@@ -243,7 +349,6 @@
     ) {
       value = value[0] || null
     }
-
     const changed = fieldApi.setValue(value)
     if (onChange && changed) {
       onChange({
@@ -251,12 +356,6 @@
       })
     }
   }
-
-  const loadMore = () => {
-    if (!$fetch.loading) {
-      fetch.nextPage()
-    }
-  }
 </script>
 
 <Field
@@ -265,31 +364,31 @@
   {disabled}
   {readonly}
   {validation}
-  {defaultValue}
   {type}
   {span}
   {helpText}
+  defaultValue={enrichedDefaultValue}
   bind:fieldState
   bind:fieldApi
   bind:fieldSchema
 >
   {#if fieldState}
     <svelte:component
-      this={component}
-      options={enrichedOptions}
-      {autocomplete}
-      value={castSelectedValue}
-      on:change={handleChange}
-      on:loadMore={loadMore}
-      id={fieldState.fieldId}
-      disabled={fieldState.disabled}
-      readonly={fieldState.readonly}
-      getOptionLabel={getDisplayName}
+      this={multiselect ? CoreMultiselect : CoreSelect}
+      value={displayValue}
+      id={fieldState?.fieldId}
+      disabled={fieldState?.disabled}
+      readonly={fieldState?.readonly}
+      loading={!!$fetch?.loading}
+      getOptionLabel={option => option.primaryDisplay}
       getOptionValue={option => option._id}
+      {options}
       {placeholder}
+      {autocomplete}
       bind:searchTerm
-      loading={$fetch.loading}
       bind:open
+      on:change={handleChange}
+      on:loadMore={() => fetch?.nextPage()}
     />
   {/if}
 </Field>
diff --git a/packages/frontend-core/src/fetch/GroupUserFetch.ts b/packages/frontend-core/src/fetch/GroupUserFetch.ts
index 5b07e9decb..ca28a4dfa1 100644
--- a/packages/frontend-core/src/fetch/GroupUserFetch.ts
+++ b/packages/frontend-core/src/fetch/GroupUserFetch.ts
@@ -4,7 +4,7 @@ import { GroupUserDatasource, InternalTable } from "@budibase/types"
 
 interface GroupUserQuery {
   groupId: string
-  emailSearch: string
+  emailSearch?: string
 }
 
 interface GroupUserDefinition {
diff --git a/packages/frontend-core/src/fetch/UserFetch.ts b/packages/frontend-core/src/fetch/UserFetch.ts
index e72ed8997d..995071b587 100644
--- a/packages/frontend-core/src/fetch/UserFetch.ts
+++ b/packages/frontend-core/src/fetch/UserFetch.ts
@@ -9,8 +9,8 @@ import {
 } from "@budibase/types"
 
 interface UserFetchQuery {
-  appId: string
-  paginated: boolean
+  appId?: string
+  paginated?: boolean
 }
 
 interface UserDefinition {
diff --git a/packages/server/package.json b/packages/server/package.json
index 9a70ecba9c..38dd746c4f 100644
--- a/packages/server/package.json
+++ b/packages/server/package.json
@@ -156,6 +156,7 @@
     "@types/pouchdb": "6.4.2",
     "@types/server-destroy": "1.0.1",
     "@types/supertest": "2.0.14",
+    "@types/swagger-jsdoc": "^6.0.4",
     "@types/tar": "6.1.5",
     "@types/tmp": "0.2.6",
     "@types/uuid": "8.3.4",
diff --git a/packages/server/specs/generate.ts b/packages/server/specs/generate.ts
index 8f6376195f..1176f187a7 100644
--- a/packages/server/specs/generate.ts
+++ b/packages/server/specs/generate.ts
@@ -4,11 +4,11 @@ import { examples, schemas } from "./resources"
 import * as parameters from "./parameters"
 import * as security from "./security"
 
-const swaggerJsdoc = require("swagger-jsdoc")
+import swaggerJsdoc from "swagger-jsdoc"
 
 const VARIABLES = {}
 
-const options = {
+const opts: swaggerJsdoc.Options = {
   definition: {
     openapi: "3.0.0",
     info: {
@@ -58,30 +58,27 @@ const options = {
 }
 
 function writeFile(output: any, filename: string) {
-  try {
-    const path = join(__dirname, filename)
-    let spec = output
-    if (filename.endsWith("json")) {
-      spec = JSON.stringify(output, null, 2)
-    }
-    // input the static variables
-    for (let [key, replacement] of Object.entries(VARIABLES)) {
-      spec = spec.replace(new RegExp(`{${key}}`, "g"), replacement)
-    }
-    writeFileSync(path, spec)
-    console.log(`Wrote spec to ${path}`)
-    return path
-  } catch (err) {
-    console.error("Error writing spec file", err)
+  const path = join(__dirname, filename)
+  let spec = output
+  if (filename.endsWith("json")) {
+    spec = JSON.stringify(output, null, 2)
   }
+  // input the static variables
+  for (let [key, replacement] of Object.entries(VARIABLES)) {
+    spec = spec.replace(new RegExp(`{${key}}`, "g"), replacement)
+  }
+  writeFileSync(path, spec)
+  console.log(`Wrote spec to ${path}`)
+  return path
+}
+
+export function spec() {
+  return swaggerJsdoc({ ...opts, format: ".json" })
 }
 
 export function run() {
-  const outputJSON = swaggerJsdoc(options)
-  options.format = ".yaml"
-  const outputYAML = swaggerJsdoc(options)
-  writeFile(outputJSON, "openapi.json")
-  return writeFile(outputYAML, "openapi.yaml")
+  writeFile(swaggerJsdoc({ ...opts, format: ".json" }), "openapi.json")
+  return writeFile(swaggerJsdoc({ ...opts, format: ".yaml" }), "openapi.yaml")
 }
 
 if (require.main === module) {
diff --git a/packages/server/specs/resources/error.ts b/packages/server/specs/resources/error.ts
new file mode 100644
index 0000000000..0d42963b73
--- /dev/null
+++ b/packages/server/specs/resources/error.ts
@@ -0,0 +1,21 @@
+import { object } from "./utils"
+import Resource from "./utils/Resource"
+
+const errorSchema = object({
+  status: {
+    type: "number",
+    description: "The HTTP status code of the error.",
+  },
+  message: {
+    type: "string",
+    description: "A descriptive message about the error.",
+  },
+})
+
+export default new Resource()
+  .setExamples({
+    error: {},
+  })
+  .setSchemas({
+    error: errorSchema,
+  })
diff --git a/packages/server/src/api/controllers/public/users.ts b/packages/server/src/api/controllers/public/users.ts
index 4265c7ac22..c0cd3248a2 100644
--- a/packages/server/src/api/controllers/public/users.ts
+++ b/packages/server/src/api/controllers/public/users.ts
@@ -48,7 +48,7 @@ function getUser(ctx: UserCtx, userId?: string) {
   if (userId) {
     ctx.params = { userId }
   } else if (!ctx.params?.userId) {
-    throw "No user ID provided for getting"
+    throw new Error("No user ID provided for getting")
   }
   return readGlobalUser(ctx)
 }
diff --git a/packages/server/src/api/routes/public/index.ts b/packages/server/src/api/routes/public/index.ts
index 531192811c..8e4533f156 100644
--- a/packages/server/src/api/routes/public/index.ts
+++ b/packages/server/src/api/routes/public/index.ts
@@ -12,6 +12,7 @@ import { paramResource, paramSubResource } from "../../../middleware/resourceId"
 import { PermissionLevel, PermissionType } from "@budibase/types"
 import { CtxFn } from "./utils/Endpoint"
 import mapperMiddleware from "./middleware/mapper"
+import testErrorHandling from "./middleware/testErrorHandling"
 import env from "../../../environment"
 import { middleware, redis } from "@budibase/backend-core"
 import { SelectableDatabase } from "@budibase/backend-core/src/redis/utils"
@@ -144,6 +145,10 @@ function applyRoutes(
   // add the output mapper middleware
   addMiddleware(endpoints.read, mapperMiddleware, { output: true })
   addMiddleware(endpoints.write, mapperMiddleware, { output: true })
+  if (env.isTest()) {
+    addMiddleware(endpoints.read, testErrorHandling())
+    addMiddleware(endpoints.write, testErrorHandling())
+  }
   addToRouter(endpoints.read)
   addToRouter(endpoints.write)
 }
diff --git a/packages/server/src/api/routes/public/middleware/testErrorHandling.ts b/packages/server/src/api/routes/public/middleware/testErrorHandling.ts
new file mode 100644
index 0000000000..b22acae8a8
--- /dev/null
+++ b/packages/server/src/api/routes/public/middleware/testErrorHandling.ts
@@ -0,0 +1,28 @@
+import { Ctx } from "@budibase/types"
+import environment from "../../../../environment"
+
+export default () => {
+  if (!environment.isTest()) {
+    throw new Error("This middleware is only for testing")
+  }
+
+  return async (ctx: Ctx, next: any) => {
+    try {
+      await next()
+    } catch (err: any) {
+      if (!ctx.headers["x-budibase-include-stacktrace"]) {
+        throw err
+      }
+
+      const status = err.status || err.statusCode || 500
+
+      let error = err
+      while (error.cause) {
+        error = error.cause
+      }
+
+      ctx.status = status
+      ctx.body = { status, message: error.message, stack: error.stack }
+    }
+  }
+}
diff --git a/packages/server/src/api/routes/public/tests/compare.spec.ts b/packages/server/src/api/routes/public/tests/compare.spec.ts
index ccf248f360..b4f5f20e2c 100644
--- a/packages/server/src/api/routes/public/tests/compare.spec.ts
+++ b/packages/server/src/api/routes/public/tests/compare.spec.ts
@@ -2,184 +2,174 @@ import jestOpenAPI from "jest-openapi"
 import { run as generateSchema } from "../../../../../specs/generate"
 import * as setup from "../../tests/utilities"
 import { generateMakeRequest } from "./utils"
-import { Table, App, Row, User } from "@budibase/types"
+import { Table, App, Row } from "@budibase/types"
+import nock from "nock"
+import environment from "../../../../environment"
 
 const yamlPath = generateSchema()
 jestOpenAPI(yamlPath!)
 
-let config = setup.getConfig()
-let apiKey: string, table: Table, app: App, makeRequest: any
+describe("compare", () => {
+  let config = setup.getConfig()
+  let apiKey: string, table: Table, app: App, makeRequest: any
 
-beforeAll(async () => {
-  app = await config.init()
-  table = await config.upsertTable()
-  apiKey = await config.generateApiKey()
-  makeRequest = generateMakeRequest(apiKey)
-})
-
-afterAll(setup.afterAll)
-
-describe("check the applications endpoints", () => {
-  it("should allow retrieving applications through search", async () => {
-    const res = await makeRequest("post", "/applications/search")
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow creating an application", async () => {
-    const res = await makeRequest(
-      "post",
-      "/applications",
-      {
-        name: "new App",
-      },
-      null
-    )
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow updating an application", async () => {
-    const app = config.getApp()
-    const appId = config.getAppId()
-    const res = await makeRequest(
-      "put",
-      `/applications/${appId}`,
-      {
-        ...app,
-        name: "updated app name",
-      },
-      appId
-    )
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow retrieving an application", async () => {
-    const res = await makeRequest("get", `/applications/${config.getAppId()}`)
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow deleting an application", async () => {
-    const res = await makeRequest(
-      "delete",
-      `/applications/${config.getAppId()}`
-    )
-    expect(res).toSatisfyApiSpec()
-  })
-})
-
-describe("check the tables endpoints", () => {
-  it("should allow retrieving tables through search", async () => {
-    await config.createApp("new app 1")
+  beforeAll(async () => {
+    app = await config.init()
     table = await config.upsertTable()
-    const res = await makeRequest("post", "/tables/search")
-    expect(res).toSatisfyApiSpec()
+    apiKey = await config.generateApiKey()
+    makeRequest = generateMakeRequest(apiKey)
   })
 
-  it("should allow creating a table", async () => {
-    const res = await makeRequest("post", "/tables", {
-      name: "table name",
-      primaryDisplay: "column1",
-      schema: {
-        column1: {
-          type: "string",
-          constraints: {},
+  afterAll(setup.afterAll)
+
+  beforeEach(() => {
+    nock.cleanAll()
+  })
+
+  describe("check the applications endpoints", () => {
+    it("should allow retrieving applications through search", async () => {
+      const res = await makeRequest("post", "/applications/search")
+      expect(res).toSatisfyApiSpec()
+    })
+
+    it("should allow creating an application", async () => {
+      const res = await makeRequest(
+        "post",
+        "/applications",
+        {
+          name: "new App",
         },
-      },
+        null
+      )
+      expect(res).toSatisfyApiSpec()
     })
-    expect(res).toSatisfyApiSpec()
-  })
 
-  it("should allow updating a table", async () => {
-    const updated = { ...table, _rev: undefined, name: "new name" }
-    const res = await makeRequest("put", `/tables/${table._id}`, updated)
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow retrieving a table", async () => {
-    const res = await makeRequest("get", `/tables/${table._id}`)
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow deleting a table", async () => {
-    const res = await makeRequest("delete", `/tables/${table._id}`)
-    expect(res).toSatisfyApiSpec()
-  })
-})
-
-describe("check the rows endpoints", () => {
-  let row: Row
-  it("should allow retrieving rows through search", async () => {
-    table = await config.upsertTable()
-    const res = await makeRequest("post", `/tables/${table._id}/rows/search`, {
-      query: {},
+    it("should allow updating an application", async () => {
+      const app = config.getApp()
+      const appId = config.getAppId()
+      const res = await makeRequest(
+        "put",
+        `/applications/${appId}`,
+        {
+          ...app,
+          name: "updated app name",
+        },
+        appId
+      )
+      expect(res).toSatisfyApiSpec()
     })
-    expect(res).toSatisfyApiSpec()
-  })
 
-  it("should allow creating a row", async () => {
-    const res = await makeRequest("post", `/tables/${table._id}/rows`, {
-      name: "test row",
+    it("should allow retrieving an application", async () => {
+      const res = await makeRequest("get", `/applications/${config.getAppId()}`)
+      expect(res).toSatisfyApiSpec()
+    })
+
+    it("should allow deleting an application", async () => {
+      nock(environment.WORKER_URL!)
+        .delete(`/api/global/roles/${config.getProdAppId()}`)
+        .reply(200, {})
+
+      const res = await makeRequest(
+        "delete",
+        `/applications/${config.getAppId()}`
+      )
+      expect(res).toSatisfyApiSpec()
     })
-    expect(res).toSatisfyApiSpec()
-    row = res.body.data
   })
 
-  it("should allow updating a row", async () => {
-    const res = await makeRequest(
-      "put",
-      `/tables/${table._id}/rows/${row._id}`,
-      {
-        name: "test row updated",
-      }
-    )
-    expect(res).toSatisfyApiSpec()
+  describe("check the tables endpoints", () => {
+    it("should allow retrieving tables through search", async () => {
+      await config.createApp("new app 1")
+      table = await config.upsertTable()
+      const res = await makeRequest("post", "/tables/search")
+      expect(res).toSatisfyApiSpec()
+    })
+
+    it("should allow creating a table", async () => {
+      const res = await makeRequest("post", "/tables", {
+        name: "table name",
+        primaryDisplay: "column1",
+        schema: {
+          column1: {
+            type: "string",
+            constraints: {},
+          },
+        },
+      })
+      expect(res).toSatisfyApiSpec()
+    })
+
+    it("should allow updating a table", async () => {
+      const updated = { ...table, _rev: undefined, name: "new name" }
+      const res = await makeRequest("put", `/tables/${table._id}`, updated)
+      expect(res).toSatisfyApiSpec()
+    })
+
+    it("should allow retrieving a table", async () => {
+      const res = await makeRequest("get", `/tables/${table._id}`)
+      expect(res).toSatisfyApiSpec()
+    })
+
+    it("should allow deleting a table", async () => {
+      const res = await makeRequest("delete", `/tables/${table._id}`)
+      expect(res).toSatisfyApiSpec()
+    })
   })
 
-  it("should allow retrieving a row", async () => {
-    const res = await makeRequest("get", `/tables/${table._id}/rows/${row._id}`)
-    expect(res).toSatisfyApiSpec()
+  describe("check the rows endpoints", () => {
+    let row: Row
+    it("should allow retrieving rows through search", async () => {
+      table = await config.upsertTable()
+      const res = await makeRequest(
+        "post",
+        `/tables/${table._id}/rows/search`,
+        {
+          query: {},
+        }
+      )
+      expect(res).toSatisfyApiSpec()
+    })
+
+    it("should allow creating a row", async () => {
+      const res = await makeRequest("post", `/tables/${table._id}/rows`, {
+        name: "test row",
+      })
+      expect(res).toSatisfyApiSpec()
+      row = res.body.data
+    })
+
+    it("should allow updating a row", async () => {
+      const res = await makeRequest(
+        "put",
+        `/tables/${table._id}/rows/${row._id}`,
+        {
+          name: "test row updated",
+        }
+      )
+      expect(res).toSatisfyApiSpec()
+    })
+
+    it("should allow retrieving a row", async () => {
+      const res = await makeRequest(
+        "get",
+        `/tables/${table._id}/rows/${row._id}`
+      )
+      expect(res).toSatisfyApiSpec()
+    })
+
+    it("should allow deleting a row", async () => {
+      const res = await makeRequest(
+        "delete",
+        `/tables/${table._id}/rows/${row._id}`
+      )
+      expect(res).toSatisfyApiSpec()
+    })
   })
 
-  it("should allow deleting a row", async () => {
-    const res = await makeRequest(
-      "delete",
-      `/tables/${table._id}/rows/${row._id}`
-    )
-    expect(res).toSatisfyApiSpec()
-  })
-})
-
-describe("check the users endpoints", () => {
-  let user: User
-  it("should allow retrieving users through search", async () => {
-    user = await config.createUser()
-    const res = await makeRequest("post", "/users/search")
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow creating a user", async () => {
-    const res = await makeRequest("post", "/users")
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow updating a user", async () => {
-    const res = await makeRequest("put", `/users/${user._id}`)
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow retrieving a user", async () => {
-    const res = await makeRequest("get", `/users/${user._id}`)
-    expect(res).toSatisfyApiSpec()
-  })
-
-  it("should allow deleting a user", async () => {
-    const res = await makeRequest("delete", `/users/${user._id}`)
-    expect(res).toSatisfyApiSpec()
-  })
-})
-
-describe("check the queries endpoints", () => {
-  it("should allow retrieving queries through search", async () => {
-    const res = await makeRequest("post", "/queries/search")
-    expect(res).toSatisfyApiSpec()
+  describe("check the queries endpoints", () => {
+    it("should allow retrieving queries through search", async () => {
+      const res = await makeRequest("post", "/queries/search")
+      expect(res).toSatisfyApiSpec()
+    })
   })
 })
diff --git a/packages/server/src/api/routes/public/tests/users.spec.ts b/packages/server/src/api/routes/public/tests/users.spec.ts
index 4ca9ff8104..bb3e4b6fba 100644
--- a/packages/server/src/api/routes/public/tests/users.spec.ts
+++ b/packages/server/src/api/routes/public/tests/users.spec.ts
@@ -1,132 +1,143 @@
 import * as setup from "../../tests/utilities"
-import { generateMakeRequest, MakeRequestResponse } from "./utils"
 import { User } from "@budibase/types"
-import { mocks } from "@budibase/backend-core/tests"
+import { generator, mocks } from "@budibase/backend-core/tests"
+import nock from "nock"
+import TestConfiguration from "../../../../tests/utilities/TestConfiguration"
+import { mockWorkerUserAPI } from "./utils"
 
-import * as workerRequests from "../../../../utilities/workerRequests"
+describe("public users API", () => {
+  const config = new TestConfiguration()
+  let globalUser: User
 
-const mockedWorkerReq = jest.mocked(workerRequests)
-
-let config = setup.getConfig()
-let apiKey: string, globalUser: User, makeRequest: MakeRequestResponse
-
-beforeAll(async () => {
-  await config.init()
-  globalUser = await config.globalUser()
-  apiKey = await config.generateApiKey(globalUser._id)
-  makeRequest = generateMakeRequest(apiKey)
-  mockedWorkerReq.readGlobalUser.mockImplementation(() =>
-    Promise.resolve(globalUser)
-  )
-})
-
-afterAll(setup.afterAll)
-
-function base() {
-  return {
-    tenantId: config.getTenantId(),
-    firstName: "Test",
-    lastName: "Test",
-  }
-}
-
-function updateMock() {
-  mockedWorkerReq.readGlobalUser.mockImplementation(ctx => ctx.request.body)
-}
-
-describe("check user endpoints", () => {
-  it("should not allow a user to update their own roles", async () => {
-    const res = await makeRequest("put", `/users/${globalUser._id}`, {
-      ...globalUser,
-      roles: {
-        app_1: "ADMIN",
-      },
-    })
-    expect(
-      mockedWorkerReq.saveGlobalUser.mock.lastCall?.[0].body.data.roles["app_1"]
-    ).toBeUndefined()
-    expect(res.status).toBe(200)
-    expect(res.body.data.roles["app_1"]).toBeUndefined()
+  beforeAll(async () => {
+    await config.init()
   })
 
-  it("should not allow a user to delete themselves", async () => {
-    const res = await makeRequest("delete", `/users/${globalUser._id}`)
-    expect(res.status).toBe(405)
-    expect(mockedWorkerReq.deleteGlobalUser.mock.lastCall).toBeUndefined()
-  })
-})
-
-describe("no user role update in free", () => {
-  beforeAll(() => {
-    updateMock()
-  })
-
-  it("should not allow 'roles' to be updated", async () => {
-    const res = await makeRequest("post", "/users", {
-      ...base(),
-      roles: { app_a: "BASIC" },
-    })
-    expect(res.status).toBe(200)
-    expect(res.body.data.roles["app_a"]).toBeUndefined()
-    expect(res.body.message).toBeDefined()
-  })
-
-  it("should not allow 'admin' to be updated", async () => {
-    const res = await makeRequest("post", "/users", {
-      ...base(),
-      admin: { global: true },
-    })
-    expect(res.status).toBe(200)
-    expect(res.body.data.admin).toBeUndefined()
-    expect(res.body.message).toBeDefined()
-  })
-
-  it("should not allow 'builder' to be updated", async () => {
-    const res = await makeRequest("post", "/users", {
-      ...base(),
-      builder: { global: true },
-    })
-    expect(res.status).toBe(200)
-    expect(res.body.data.builder).toBeUndefined()
-    expect(res.body.message).toBeDefined()
-  })
-})
-
-describe("no user role update in business", () => {
-  beforeAll(() => {
-    updateMock()
-    mocks.licenses.useExpandedPublicApi()
-  })
-
-  it("should allow 'roles' to be updated", async () => {
-    const res = await makeRequest("post", "/users", {
-      ...base(),
-      roles: { app_a: "BASIC" },
-    })
-    expect(res.status).toBe(200)
-    expect(res.body.data.roles["app_a"]).toBe("BASIC")
-    expect(res.body.message).toBeUndefined()
-  })
-
-  it("should allow 'admin' to be updated", async () => {
-    mocks.licenses.useExpandedPublicApi()
-    const res = await makeRequest("post", "/users", {
-      ...base(),
-      admin: { global: true },
-    })
-    expect(res.status).toBe(200)
-    expect(res.body.data.admin.global).toBe(true)
-    expect(res.body.message).toBeUndefined()
-  })
-
-  it("should allow 'builder' to be updated", async () => {
-    mocks.licenses.useExpandedPublicApi()
-    const res = await makeRequest("post", "/users", {
-      ...base(),
-      builder: { global: true },
-    })
-    expect(res.status).toBe(200)
-    expect(res.body.data.builder.global).toBe(true)
-    expect(res.body.message).toBeUndefined()
+  afterAll(setup.afterAll)
+
+  beforeEach(async () => {
+    globalUser = await config.globalUser()
+
+    nock.cleanAll()
+    mockWorkerUserAPI(globalUser)
+  })
+
+  describe("read", () => {
+    it("should allow a user to read themselves", async () => {
+      const user = await config.api.user.find(globalUser._id!)
+      expect(user._id).toBe(globalUser._id)
+    })
+
+    it("should allow a user to read another user", async () => {
+      const otherUser = await config.api.public.user.create({
+        email: generator.email({ domain: "example.com" }),
+        roles: {},
+      })
+      const user = await config.withUser(globalUser, () =>
+        config.api.public.user.find(otherUser._id!)
+      )
+      expect(user._id).toBe(otherUser._id)
+    })
+  })
+
+  describe("create", () => {
+    it("can successfully create a new user", async () => {
+      const email = generator.email({ domain: "example.com" })
+      const newUser = await config.api.public.user.create({
+        email,
+        roles: {},
+      })
+      expect(newUser.email).toBe(email)
+      expect(newUser._id).toBeDefined()
+    })
+
+    describe("role creation on free tier", () => {
+      it("should not allow 'roles' to be updated", async () => {
+        const newUser = await config.api.public.user.create({
+          email: generator.email({ domain: "example.com" }),
+          roles: { app_a: "BASIC" },
+        })
+        expect(newUser.roles["app_a"]).toBeUndefined()
+      })
+
+      it("should not allow 'admin' to be updated", async () => {
+        const newUser = await config.api.public.user.create({
+          email: generator.email({ domain: "example.com" }),
+          roles: {},
+          admin: { global: true },
+        })
+        expect(newUser.admin).toBeUndefined()
+      })
+
+      it("should not allow 'builder' to be updated", async () => {
+        const newUser = await config.api.public.user.create({
+          email: generator.email({ domain: "example.com" }),
+          roles: {},
+          builder: { global: true },
+        })
+        expect(newUser.builder).toBeUndefined()
+      })
+    })
+
+    describe("role creation on business tier", () => {
+      beforeAll(() => {
+        mocks.licenses.useExpandedPublicApi()
+      })
+
+      it("should allow 'roles' to be updated", async () => {
+        const newUser = await config.api.public.user.create({
+          email: generator.email({ domain: "example.com" }),
+          roles: { app_a: "BASIC" },
+        })
+        expect(newUser.roles["app_a"]).toBe("BASIC")
+      })
+
+      it("should allow 'admin' to be updated", async () => {
+        const newUser = await config.api.public.user.create({
+          email: generator.email({ domain: "example.com" }),
+          roles: {},
+          admin: { global: true },
+        })
+        expect(newUser.admin?.global).toBe(true)
+      })
+
+      it("should allow 'builder' to be updated", async () => {
+        const newUser = await config.api.public.user.create({
+          email: generator.email({ domain: "example.com" }),
+          roles: {},
+          builder: { global: true },
+        })
+        expect(newUser.builder?.global).toBe(true)
+      })
+    })
+  })
+
+  describe("update", () => {
+    it("can update a user", async () => {
+      const updatedUser = await config.api.public.user.update({
+        ...globalUser,
+        email: `updated-${globalUser.email}`,
+      })
+      expect(updatedUser.email).toBe(`updated-${globalUser.email}`)
+    })
+
+    it("should not allow a user to update their own roles", async () => {
+      await config.withUser(globalUser, () =>
+        config.api.public.user.update({
+          ...globalUser,
+          roles: { app_1: "ADMIN" },
+        })
+      )
+      const updatedUser = await config.api.user.find(globalUser._id!)
+      expect(updatedUser.roles?.app_1).toBeUndefined()
+    })
+  })
+
+  describe("delete", () => {
+    it("should not allow a user to delete themselves", async () => {
+      await config.withUser(globalUser, () =>
+        config.api.public.user.destroy(globalUser._id!, { status: 405 })
+      )
+    })
   })
 })
diff --git a/packages/server/src/api/routes/public/tests/utils.ts b/packages/server/src/api/routes/public/tests/utils.ts
index 4fb048a540..4985c0db58 100644
--- a/packages/server/src/api/routes/public/tests/utils.ts
+++ b/packages/server/src/api/routes/public/tests/utils.ts
@@ -1,6 +1,10 @@
 import * as setup from "../../tests/utilities"
 import { checkSlashesInUrl } from "../../../../utilities"
 import supertest from "supertest"
+import { User } from "@budibase/types"
+import environment from "../../../../environment"
+import nock from "nock"
+import { generator } from "@budibase/backend-core/tests"
 
 export type HttpMethod = "post" | "get" | "put" | "delete" | "patch"
 
@@ -91,3 +95,43 @@ export function generateMakeRequestWithFormData(
     return res
   }
 }
+
+export function mockWorkerUserAPI(...seedUsers: User[]) {
+  const users: Record<string, User> = {
+    ...seedUsers.reduce((acc, user) => {
+      acc[user._id!] = user
+      return acc
+    }, {} as Record<string, User>),
+  }
+
+  nock(environment.WORKER_URL!)
+    .get(new RegExp(`/api/global/users/.*`))
+    .reply(200, (uri, body) => {
+      const id = uri.split("/").pop()
+      return users[id!]
+    })
+    .persist()
+
+  nock(environment.WORKER_URL!)
+    .post(`/api/global/users`)
+    .reply(200, (uri, body) => {
+      const newUser = body as User
+      if (!newUser._id) {
+        newUser._id = `us_${generator.guid()}`
+      }
+      users[newUser._id!] = newUser
+      return newUser
+    })
+    .persist()
+
+  nock(environment.WORKER_URL!)
+    .put(new RegExp(`/api/global/users/.*`))
+    .reply(200, (uri, body) => {
+      const id = uri.split("/").pop()!
+      const updatedUser = body as User
+      const existingUser = users[id] || {}
+      users[id] = { ...existingUser, ...updatedUser }
+      return users[id]
+    })
+    .persist()
+}
diff --git a/packages/server/src/api/routes/tests/utilities/index.ts b/packages/server/src/api/routes/tests/utilities/index.ts
index dcb8ccd6c0..944a56d7ba 100644
--- a/packages/server/src/api/routes/tests/utilities/index.ts
+++ b/packages/server/src/api/routes/tests/utilities/index.ts
@@ -3,44 +3,6 @@ import supertest from "supertest"
 
 export * as structures from "../../../../tests/utilities/structures"
 
-function user() {
-  return {
-    _id: "user",
-    _rev: "rev",
-    createdAt: Date.now(),
-    email: "test@example.com",
-    roles: {},
-    tenantId: "default",
-    status: "active",
-  }
-}
-
-jest.mock("../../../../utilities/workerRequests", () => ({
-  getGlobalUsers: jest.fn(() => {
-    return {
-      _id: "us_uuid1",
-    }
-  }),
-  getGlobalSelf: jest.fn(() => {
-    return {
-      _id: "us_uuid1",
-    }
-  }),
-  allGlobalUsers: jest.fn(() => {
-    return [user()]
-  }),
-  readGlobalUser: jest.fn(() => {
-    return user()
-  }),
-  saveGlobalUser: jest.fn(() => {
-    return { _id: "user", _rev: "rev" }
-  }),
-  deleteGlobalUser: jest.fn(() => {
-    return { message: "deleted user" }
-  }),
-  removeAppFromUserRoles: jest.fn(),
-}))
-
 export function delay(ms: number) {
   return new Promise(resolve => setTimeout(resolve, ms))
 }
diff --git a/packages/server/src/tests/utilities/TestConfiguration.ts b/packages/server/src/tests/utilities/TestConfiguration.ts
index 0d1330b4f4..273760cb34 100644
--- a/packages/server/src/tests/utilities/TestConfiguration.ts
+++ b/packages/server/src/tests/utilities/TestConfiguration.ts
@@ -67,6 +67,7 @@ import {
   View,
   Webhook,
   WithRequired,
+  DevInfo,
 } from "@budibase/types"
 
 import API from "./api"
@@ -249,7 +250,7 @@ export default class TestConfiguration {
     }
   }
 
-  async withUser(user: User, f: () => Promise<void>) {
+  async withUser<T>(user: User, f: () => Promise<T>): Promise<T> {
     const oldUser = this.user
     this.user = user
     try {
@@ -470,7 +471,10 @@ export default class TestConfiguration {
     }
   }
 
-  defaultHeaders(extras = {}, prodApp = false) {
+  defaultHeaders(
+    extras: Record<string, string | string[]> = {},
+    prodApp = false
+  ) {
     const tenantId = this.getTenantId()
     const user = this.getUser()
     const authObj: AuthToken = {
@@ -499,10 +503,13 @@ export default class TestConfiguration {
     }
   }
 
-  publicHeaders({ prodApp = true } = {}) {
+  publicHeaders({
+    prodApp = true,
+    extras = {},
+  }: { prodApp?: boolean; extras?: Record<string, string | string[]> } = {}) {
     const appId = prodApp ? this.prodAppId : this.appId
 
-    const headers: any = {
+    const headers: Record<string, string> = {
       Accept: "application/json",
       Cookie: "",
     }
@@ -515,6 +522,7 @@ export default class TestConfiguration {
     return {
       ...headers,
       ...this.temporaryHeaders,
+      ...extras,
     }
   }
 
@@ -578,17 +586,17 @@ export default class TestConfiguration {
     }
     const db = tenancy.getTenantDB(this.getTenantId())
     const id = dbCore.generateDevInfoID(userId)
-    let devInfo: any
-    try {
-      devInfo = await db.get(id)
-    } catch (err) {
-      devInfo = { _id: id, userId }
+    const devInfo = await db.tryGet<DevInfo>(id)
+    if (devInfo && devInfo.apiKey) {
+      return devInfo.apiKey
     }
-    devInfo.apiKey = encryption.encrypt(
+
+    const apiKey = encryption.encrypt(
       `${this.getTenantId()}${dbCore.SEPARATOR}${newid()}`
     )
-    await db.put(devInfo)
-    return devInfo.apiKey
+    const newDevInfo: DevInfo = { _id: id, userId, apiKey }
+    await db.put(newDevInfo)
+    return apiKey
   }
 
   // APP
diff --git a/packages/server/src/tests/utilities/api/base.ts b/packages/server/src/tests/utilities/api/base.ts
index 39ac5cefc0..9b47cfb820 100644
--- a/packages/server/src/tests/utilities/api/base.ts
+++ b/packages/server/src/tests/utilities/api/base.ts
@@ -1,8 +1,12 @@
+import jestOpenAPI from "jest-openapi"
+import { spec } from "../../../../specs/generate"
 import TestConfiguration from "../TestConfiguration"
 import request, { SuperTest, Test, Response } from "supertest"
 import { ReadStream } from "fs"
 import { getServer } from "../../../app"
 
+jestOpenAPI(spec() as any)
+
 type Headers = Record<string, string | string[] | undefined>
 type Method = "get" | "post" | "put" | "patch" | "delete"
 
@@ -46,6 +50,7 @@ export interface RequestOpts {
 export abstract class TestAPI {
   config: TestConfiguration
   request: SuperTest<Test>
+  prefix = ""
 
   constructor(config: TestConfiguration) {
     this.config = config
@@ -53,26 +58,26 @@ export abstract class TestAPI {
   }
 
   protected _get = async <T>(url: string, opts?: RequestOpts): Promise<T> => {
-    return await this._request<T>("get", url, opts)
+    return await this._request<T>("get", `${this.prefix}${url}`, opts)
   }
 
   protected _post = async <T>(url: string, opts?: RequestOpts): Promise<T> => {
-    return await this._request<T>("post", url, opts)
+    return await this._request<T>("post", `${this.prefix}${url}`, opts)
   }
 
   protected _put = async <T>(url: string, opts?: RequestOpts): Promise<T> => {
-    return await this._request<T>("put", url, opts)
+    return await this._request<T>("put", `${this.prefix}${url}`, opts)
   }
 
   protected _patch = async <T>(url: string, opts?: RequestOpts): Promise<T> => {
-    return await this._request<T>("patch", url, opts)
+    return await this._request<T>("patch", `${this.prefix}${url}`, opts)
   }
 
   protected _delete = async <T>(
     url: string,
     opts?: RequestOpts
   ): Promise<T> => {
-    return await this._request<T>("delete", url, opts)
+    return await this._request<T>("delete", `${this.prefix}${url}`, opts)
   }
 
   protected _requestRaw = async (
@@ -88,7 +93,6 @@ export abstract class TestAPI {
       fields = {},
       files = {},
       expectations,
-      publicUser = false,
     } = opts || {}
     const { status = 200 } = expectations || {}
     const expectHeaders = expectations?.headers || {}
@@ -97,7 +101,7 @@ export abstract class TestAPI {
       expectHeaders["Content-Type"] = /^application\/json/
     }
 
-    let queryParams = []
+    let queryParams: string[] = []
     for (const [key, value] of Object.entries(query)) {
       if (value) {
         queryParams.push(`${key}=${value}`)
@@ -107,18 +111,10 @@ export abstract class TestAPI {
       url += `?${queryParams.join("&")}`
     }
 
-    const headersFn = publicUser
-      ? (_extras = {}) =>
-          this.config.publicHeaders.bind(this.config)({
-            prodApp: opts?.useProdApp,
-          })
-      : (extras = {}) =>
-          this.config.defaultHeaders.bind(this.config)(extras, opts?.useProdApp)
-
     const app = getServer()
     let req = request(app)[method](url)
     req = req.set(
-      headersFn({
+      await this.getHeaders(opts, {
         "x-budibase-include-stacktrace": "true",
       })
     )
@@ -167,10 +163,18 @@ export abstract class TestAPI {
     }
   }
 
-  protected _checkResponse = (
-    response: Response,
-    expectations?: Expectations
-  ) => {
+  protected async getHeaders(
+    opts?: RequestOpts,
+    extras?: Record<string, string | string[]>
+  ): Promise<Record<string, string | string[]>> {
+    if (opts?.publicUser) {
+      return this.config.publicHeaders({ prodApp: opts?.useProdApp, extras })
+    } else {
+      return this.config.defaultHeaders(extras, opts?.useProdApp)
+    }
+  }
+
+  protected _checkResponse(response: Response, expectations?: Expectations) {
     const { status = 200 } = expectations || {}
 
     if (response.status !== status) {
@@ -236,3 +240,34 @@ export abstract class TestAPI {
     ).body
   }
 }
+
+export abstract class PublicAPI extends TestAPI {
+  prefix = "/api/public/v1"
+
+  protected async getHeaders(
+    opts?: RequestOpts,
+    extras?: Record<string, string | string[]>
+  ): Promise<Record<string, string | string[]>> {
+    const apiKey = await this.config.generateApiKey()
+
+    const headers: Record<string, string | string[]> = {
+      Accept: "application/json",
+      Host: this.config.tenantHost(),
+      "x-budibase-api-key": apiKey,
+      "x-budibase-app-id": this.config.getAppId(),
+      ...extras,
+    }
+
+    return headers
+  }
+
+  protected _checkResponse(response: Response, expectations?: Expectations) {
+    const checked = super._checkResponse(response, expectations)
+    if (checked.status >= 200 && checked.status < 300) {
+      // We don't seem to have documented our errors yet, so for the time being
+      // we'll only do the schema check for successful responses.
+      expect(checked).toSatisfyApiSpec()
+    }
+    return checked
+  }
+}
diff --git a/packages/server/src/tests/utilities/api/index.ts b/packages/server/src/tests/utilities/api/index.ts
index 2fdf726b6c..1252b10e40 100644
--- a/packages/server/src/tests/utilities/api/index.ts
+++ b/packages/server/src/tests/utilities/api/index.ts
@@ -17,6 +17,7 @@ import { RowActionAPI } from "./rowAction"
 import { AutomationAPI } from "./automation"
 import { PluginAPI } from "./plugin"
 import { WebhookAPI } from "./webhook"
+import { UserPublicAPI } from "./public/user"
 
 export default class API {
   application: ApplicationAPI
@@ -38,6 +39,10 @@ export default class API {
   viewV2: ViewV2API
   webhook: WebhookAPI
 
+  public: {
+    user: UserPublicAPI
+  }
+
   constructor(config: TestConfiguration) {
     this.application = new ApplicationAPI(config)
     this.attachment = new AttachmentAPI(config)
@@ -57,5 +62,8 @@ export default class API {
     this.user = new UserAPI(config)
     this.viewV2 = new ViewV2API(config)
     this.webhook = new WebhookAPI(config)
+    this.public = {
+      user: new UserPublicAPI(config),
+    }
   }
 }
diff --git a/packages/server/src/tests/utilities/api/public/user.ts b/packages/server/src/tests/utilities/api/public/user.ts
new file mode 100644
index 0000000000..4f5fccc740
--- /dev/null
+++ b/packages/server/src/tests/utilities/api/public/user.ts
@@ -0,0 +1,34 @@
+import { UnsavedUser, User } from "@budibase/types"
+import { Expectations, PublicAPI } from "../base"
+
+export class UserPublicAPI extends PublicAPI {
+  find = async (id: string, expectations?: Expectations): Promise<User> => {
+    const response = await this._get<{ data: User }>(`/users/${id}`, {
+      expectations,
+    })
+    return response.data
+  }
+
+  update = async (user: User, expectations?: Expectations): Promise<User> => {
+    const response = await this._put<{ data: User }>(`/users/${user._id}`, {
+      body: user,
+      expectations,
+    })
+    return response.data
+  }
+
+  destroy = async (id: string, expectations?: Expectations): Promise<void> => {
+    return await this._delete(`/users/${id}`, { expectations })
+  }
+
+  create = async (
+    user: UnsavedUser,
+    expectations?: Expectations
+  ): Promise<User> => {
+    const response = await this._post<{ data: User }>("/users", {
+      body: user,
+      expectations,
+    })
+    return response.data
+  }
+}
diff --git a/yarn.lock b/yarn.lock
index 279c4067a4..5173e81408 100644
--- a/yarn.lock
+++ b/yarn.lock
@@ -2796,9 +2796,9 @@
     through2 "^2.0.0"
 
 "@budibase/pro@npm:@budibase/pro@latest":
-  version "3.4.20"
-  resolved "https://registry.yarnpkg.com/@budibase/pro/-/pro-3.4.20.tgz#0d855d6ed8fe92fd178c74a8963d879cc124b034"
-  integrity sha512-hUteGvhMOKjBo0fluxcqNs7d4x8OU5W8Oqqrm7eIS9Ohe7ala2iWNCcrj+x+S9CavIm6s7JZZnAewa2Maiz2zQ==
+  version "3.4.22"
+  resolved "https://registry.yarnpkg.com/@budibase/pro/-/pro-3.4.22.tgz#943f23cb7056041bc1f433ee60b3d093145e7a4a"
+  integrity sha512-Du3iZsmRLopfoi2SvxQyY1P2Su3Nw0WbITOrKmZFsVLjZ9MzzTZs0Ph/SJHzrfJpM7rn9+8788BLSf3Z3l9KcQ==
   dependencies:
     "@anthropic-ai/sdk" "^0.27.3"
     "@budibase/backend-core" "*"
@@ -7142,6 +7142,11 @@
   dependencies:
     "@types/superagent" "*"
 
+"@types/swagger-jsdoc@^6.0.4":
+  version "6.0.4"
+  resolved "https://registry.yarnpkg.com/@types/swagger-jsdoc/-/swagger-jsdoc-6.0.4.tgz#bb4f60f3a5f103818e022f2e29ff8935113fb83d"
+  integrity sha512-W+Xw5epcOZrF/AooUM/PccNMSAFOKWZA5dasNyMujTwsBkU74njSJBpvCCJhHAJ95XRMzQrrW844Btu0uoetwQ==
+
 "@types/tar-fs@2.0.1":
   version "2.0.1"
   resolved "https://registry.yarnpkg.com/@types/tar-fs/-/tar-fs-2.0.1.tgz#6391dcad1b03dea2d79fac07371585ab54472bb1"