diff --git a/packages/server/app.ts b/packages/server/app.ts
index 56f2812be..19e6e21be 100644
--- a/packages/server/app.ts
+++ b/packages/server/app.ts
@@ -54,7 +54,6 @@ import {
 } from '@/modules/shared/helpers/envHelper'
 import * as ModulesSetup from '@/modules'
 import { GraphQLContext, Optional } from '@/modules/shared/helpers/typeHelper'
-import { createRateLimiterMiddleware } from '@/modules/core/services/ratelimiter'
 
 import { get, has, isString } from 'lodash'
 import { corsMiddlewareFactory } from '@/modules/core/configs/cors'
@@ -87,6 +86,7 @@ import {
   initiateRequestContextMiddleware
 } from '@/logging/requestContext'
 import { randomUUID } from 'crypto'
+import { createRateLimiterMiddleware } from '@/modules/core/rest/ratelimiter'
 
 const GRAPHQL_PATH = '/graphql'
 
diff --git a/packages/server/modules/auth/strategies/local.ts b/packages/server/modules/auth/strategies/local.ts
index 1bc363ea7..8ab18a339 100644
--- a/packages/server/modules/auth/strategies/local.ts
+++ b/packages/server/modules/auth/strategies/local.ts
@@ -1,5 +1,4 @@
 import {
-  sendRateLimitResponse,
   getRateLimitResult,
   isRateLimitBreached
 } from '@/modules/core/services/ratelimiter'
@@ -24,6 +23,9 @@ import {
 } from '@/modules/core/domain/users/operations'
 import { GetServerInfo } from '@/modules/core/domain/server/operations'
 import { UserValidationError } from '@/modules/core/errors/user'
+import { RateLimitError } from '@/modules/core/errors/ratelimit'
+import { isRateLimiterEnabled } from '@/modules/shared/helpers/envHelper'
+import { addRateLimitHeadersToResponse } from '@/modules/core/rest/ratelimiter'
 
 const localStrategyBuilderFactory =
   (deps: {
@@ -97,12 +99,16 @@ const localStrategyBuilderFactory =
           if (!req.body.password) throw new UserInputError('Password missing')
 
           const user = req.body
-          const ip = getIpFromRequest(req)
-          if (ip) user.ip = ip
-          const source = ip ? ip : 'unknown'
-          const rateLimitResult = await deps.getRateLimitResult('USER_CREATE', source)
-          if (isRateLimitBreached(rateLimitResult)) {
-            return sendRateLimitResponse(res, rateLimitResult)
+
+          if (isRateLimiterEnabled()) {
+            const ip = getIpFromRequest(req)
+            if (ip) user.ip = ip
+            const source = ip ? ip : 'unknown'
+            const rateLimitResult = await deps.getRateLimitResult('USER_CREATE', source)
+            if (isRateLimitBreached(rateLimitResult)) {
+              addRateLimitHeadersToResponse(res, rateLimitResult)
+              return next(new RateLimitError(rateLimitResult))
+            }
           }
 
           // 1. if the server is invite only you must have an invite
diff --git a/packages/server/modules/core/graph/resolvers/commits.ts b/packages/server/modules/core/graph/resolvers/commits.ts
index 1a8711637..795b40c28 100644
--- a/packages/server/modules/core/graph/resolvers/commits.ts
+++ b/packages/server/modules/core/graph/resolvers/commits.ts
@@ -75,6 +75,7 @@ import {
 import { LegacyUserCommit } from '@/modules/core/domain/commits/types'
 import coreModule from '@/modules/core'
 import { getEventBus } from '@/modules/shared/services/eventBus'
+import { isRateLimiterEnabled } from '@/modules/shared/helpers/envHelper'
 
 const getStreams = getStreamsFactory({ db })
 
@@ -340,9 +341,14 @@ export = {
         context.resourceAccessRules
       )
 
-      const rateLimitResult = await getRateLimitResult('COMMIT_CREATE', context.userId!)
-      if (isRateLimitBreached(rateLimitResult)) {
-        throw new RateLimitError(rateLimitResult)
+      if (isRateLimiterEnabled()) {
+        const rateLimitResult = await getRateLimitResult(
+          'COMMIT_CREATE',
+          context.userId!
+        )
+        if (isRateLimitBreached(rateLimitResult)) {
+          throw new RateLimitError(rateLimitResult)
+        }
       }
 
       const createCommitByBranchId = createCommitByBranchIdFactory({
diff --git a/packages/server/modules/core/graph/resolvers/projects.ts b/packages/server/modules/core/graph/resolvers/projects.ts
index 34df2b857..b82fd62a5 100644
--- a/packages/server/modules/core/graph/resolvers/projects.ts
+++ b/packages/server/modules/core/graph/resolvers/projects.ts
@@ -91,6 +91,7 @@ import { createAndSendInviteFactory } from '@/modules/serverinvites/services/cre
 import { inviteUsersToProjectFactory } from '@/modules/serverinvites/services/projectInviteManagement'
 import { authorizeResolver, validateScopes } from '@/modules/shared'
 import { throwForNotHavingServerRole } from '@/modules/shared/authz'
+import { isRateLimiterEnabled } from '@/modules/shared/helpers/envHelper'
 import { getEventBus } from '@/modules/shared/services/eventBus'
 import {
   filteredSubscribe,
@@ -289,9 +290,14 @@ export = {
     },
     // This one is only used outside of a workspace, so the project is always created in the main db
     async create(_parent, args, context) {
-      const rateLimitResult = await getRateLimitResult('STREAM_CREATE', context.userId!)
-      if (isRateLimitBreached(rateLimitResult)) {
-        throw new RateLimitError(rateLimitResult)
+      if (isRateLimiterEnabled()) {
+        const rateLimitResult = await getRateLimitResult(
+          'STREAM_CREATE',
+          context.userId!
+        )
+        if (isRateLimitBreached(rateLimitResult)) {
+          throw new RateLimitError(rateLimitResult)
+        }
       }
 
       const regionKey = await getValidDefaultProjectRegionKey()
diff --git a/packages/server/modules/core/graph/resolvers/streams.ts b/packages/server/modules/core/graph/resolvers/streams.ts
index c244be87b..b22983ee0 100644
--- a/packages/server/modules/core/graph/resolvers/streams.ts
+++ b/packages/server/modules/core/graph/resolvers/streams.ts
@@ -82,7 +82,10 @@ import {
 } from '@/modules/core/services/streams/favorite'
 import { getUserFactory, getUsersFactory } from '@/modules/core/repositories/users'
 import { getServerInfoFactory } from '@/modules/core/repositories/server'
-import { adminOverrideEnabled } from '@/modules/shared/helpers/envHelper'
+import {
+  adminOverrideEnabled,
+  isRateLimiterEnabled
+} from '@/modules/shared/helpers/envHelper'
 
 const getServerInfo = getServerInfoFactory({ db })
 const getUsers = getUsersFactory({ db })
@@ -435,9 +438,14 @@ export = {
   },
   Mutation: {
     async streamCreate(_, args, context) {
-      const rateLimitResult = await getRateLimitResult('STREAM_CREATE', context.userId!)
-      if (isRateLimitBreached(rateLimitResult)) {
-        throw new RateLimitError(rateLimitResult)
+      if (isRateLimiterEnabled()) {
+        const rateLimitResult = await getRateLimitResult(
+          'STREAM_CREATE',
+          context.userId!
+        )
+        if (isRateLimitBreached(rateLimitResult)) {
+          throw new RateLimitError(rateLimitResult)
+        }
       }
 
       const { id } = await createStreamReturnRecord({
diff --git a/packages/server/modules/core/graph/resolvers/versions.ts b/packages/server/modules/core/graph/resolvers/versions.ts
index 475a039fc..572df3316 100644
--- a/packages/server/modules/core/graph/resolvers/versions.ts
+++ b/packages/server/modules/core/graph/resolvers/versions.ts
@@ -5,7 +5,10 @@ import {
   filteredSubscribe,
   ProjectSubscriptions
 } from '@/modules/shared/utils/subscriptions'
-import { getServerOrigin } from '@/modules/shared/helpers/envHelper'
+import {
+  getServerOrigin,
+  isRateLimiterEnabled
+} from '@/modules/shared/helpers/envHelper'
 import {
   batchDeleteCommitsFactory,
   batchMoveCommitsFactory
@@ -169,9 +172,11 @@ export = {
         projectId: args.input.projectId
       })
 
-      const rateLimitResult = await getRateLimitResult('COMMIT_CREATE', ctx.userId!)
-      if (isRateLimitBreached(rateLimitResult)) {
-        throw new RateLimitError(rateLimitResult)
+      if (isRateLimiterEnabled()) {
+        const rateLimitResult = await getRateLimitResult('COMMIT_CREATE', ctx.userId!)
+        if (isRateLimitBreached(rateLimitResult)) {
+          throw new RateLimitError(rateLimitResult)
+        }
       }
 
       const projectDb = await getProjectDbClient({ projectId: args.input.projectId })
diff --git a/packages/server/modules/core/rest/ratelimiter.ts b/packages/server/modules/core/rest/ratelimiter.ts
new file mode 100644
index 000000000..fcb7848c3
--- /dev/null
+++ b/packages/server/modules/core/rest/ratelimiter.ts
@@ -0,0 +1,69 @@
+import type { RequestHandler, Response } from 'express'
+import {
+  getActionForPath,
+  getRateLimitResult,
+  getSourceFromRequest,
+  isRateLimitBreached,
+  RATE_LIMITERS,
+  type RateLimitBreached,
+  type RateLimiterMapping
+} from '@/modules/core/services/ratelimiter'
+import { isRateLimiterEnabled } from '@/modules/shared/helpers/envHelper'
+import { getRequestPath } from '@/modules/core/helpers/server'
+import { RateLimitError } from '@/modules/core/errors/ratelimit'
+import { ensureError } from '@speckle/shared'
+
+export const createRateLimiterMiddleware = (
+  rateLimiterMapping: RateLimiterMapping = RATE_LIMITERS
+): RequestHandler => {
+  return async (req, res, next) => {
+    if (!isRateLimiterEnabled()) return next()
+    const path = getRequestPath(req) || ''
+    const action = getActionForPath(path, req.method)
+    const source = getSourceFromRequest(req)
+    try {
+      const rateLimitResult = await getRateLimitResult(
+        action,
+        source,
+        rateLimiterMapping
+      )
+      if (isRateLimitBreached(rateLimitResult)) {
+        addRateLimitHeadersToResponse(res, rateLimitResult)
+        return next(new RateLimitError(rateLimitResult))
+      } else {
+        if (res.headersSent) return res
+        res.setHeader('X-RateLimit-Remaining', rateLimitResult.remainingPoints)
+        return next()
+      }
+    } catch (err) {
+      const e = !(err instanceof RateLimitError)
+        ? new RateLimitError(
+            {
+              isWithinLimits: false,
+              msBeforeNext: 0,
+              action
+            },
+            'Unknown rate limit error',
+            { cause: ensureError(err) }
+          )
+        : err
+
+      addRateLimitHeadersToResponse(res, e.rateLimitBreached)
+      return next(e)
+    }
+  }
+}
+
+export const addRateLimitHeadersToResponse = (
+  res: Response,
+  rateLimitBreached: RateLimitBreached
+) => {
+  if (res.headersSent) return res
+  res.setHeader('Retry-After', rateLimitBreached.msBeforeNext / 1000)
+  res.removeHeader('X-RateLimit-Remaining')
+  res.setHeader(
+    'X-RateLimit-Reset',
+    new Date(Date.now() + rateLimitBreached.msBeforeNext).toISOString()
+  )
+  res.setHeader('X-Speckle-Meditation', 'https://http.cat/429')
+}
diff --git a/packages/server/modules/core/services/ratelimiter.ts b/packages/server/modules/core/services/ratelimiter.ts
index fd490118f..792ca436f 100644
--- a/packages/server/modules/core/services/ratelimiter.ts
+++ b/packages/server/modules/core/services/ratelimiter.ts
@@ -1,9 +1,5 @@
 import express from 'express'
-import {
-  getRedisUrl,
-  getIntFromEnv,
-  getBooleanFromEnv
-} from '@/modules/shared/helpers/envHelper'
+import { getRedisUrl, getIntFromEnv } from '@/modules/shared/helpers/envHelper'
 import {
   BurstyRateLimiter,
   RateLimiterAbstract,
@@ -13,10 +9,8 @@ import {
 } from 'rate-limiter-flexible'
 import { TIME } from '@speckle/shared'
 import { getIpFromRequest } from '@/modules/shared/utils/ip'
-import { RateLimitError } from '@/modules/core/errors/ratelimit'
 import { rateLimiterLogger } from '@/logging/logging'
 import { createRedisClient } from '@/modules/shared/redis/redis'
-import { getRequestPath } from '@/modules/core/helpers/server'
 import { getTokenFromRequest } from '@/modules/shared/middleware'
 
 export interface RateLimitResult {
@@ -56,10 +50,6 @@ export type RateLimiterMapping = {
 
 export type RateLimitAction = keyof typeof LIMITS
 
-export const isRateLimiterEnabled = (): boolean => {
-  return getBooleanFromEnv('RATELIMITER_ENABLED', true)
-}
-
 export const LIMITS = <const>{
   ALL_REQUESTS: {
     regularOptions: {
@@ -272,23 +262,6 @@ export const LIMITS = <const>{
 
 export const allActions = Object.keys(LIMITS) as RateLimitAction[]
 
-export const sendRateLimitResponse = (
-  res: express.Response,
-  rateLimitBreached: RateLimitBreached
-): express.Response => {
-  if (res.headersSent) return res
-  res.setHeader('Retry-After', rateLimitBreached.msBeforeNext / 1000)
-  res.removeHeader('X-RateLimit-Remaining')
-  res.setHeader(
-    'X-RateLimit-Reset',
-    new Date(Date.now() + rateLimitBreached.msBeforeNext).toISOString()
-  )
-  res.setHeader('X-Speckle-Meditation', 'https://http.cat/429')
-  return res.status(429).send({
-    err: 'You are sending too many requests. You have been rate limited. Please try again later.'
-  })
-}
-
 export const getActionForPath = (path: string, verb: string): RateLimitAction => {
   const maybeAction = `${verb} ${path}` as RateLimitAction
   const maybeActionNoVerb = path as RateLimitAction
@@ -308,35 +281,6 @@ export const getSourceFromRequest = (req: express.Request): string => {
   return source
 }
 
-export const createRateLimiterMiddleware = (
-  rateLimiterMapping: RateLimiterMapping = RATE_LIMITERS
-) => {
-  return async (
-    req: express.Request,
-    res: express.Response,
-    next: express.NextFunction
-  ) => {
-    if (!isRateLimiterEnabled()) return next()
-    const path = getRequestPath(req) || ''
-    const action = getActionForPath(path, req.method)
-    const source = getSourceFromRequest(req)
-
-    const rateLimitResult = await getRateLimitResult(action, source, rateLimiterMapping)
-    if (isRateLimitBreached(rateLimitResult)) {
-      return sendRateLimitResponse(res, rateLimitResult)
-    } else {
-      try {
-        if (res.headersSent) return res
-        res.setHeader('X-RateLimit-Remaining', rateLimitResult.remainingPoints)
-        return next()
-      } catch (err) {
-        if (!(err instanceof RateLimitError)) throw err
-        return sendRateLimitResponse(res, err.rateLimitBreached)
-      }
-    }
-  }
-}
-
 // we need to take the `BurstyRateLimiter` specific type because
 // its not considered as an RateLimiterAbstract in the rate-limiter-flexible package
 // This is just a rant comment, but why define the Abstract then if not
diff --git a/packages/server/modules/core/tests/ratelimiter.spec.ts b/packages/server/modules/core/tests/ratelimiter.spec.ts
index 557b7241f..0318075bb 100644
--- a/packages/server/modules/core/tests/ratelimiter.spec.ts
+++ b/packages/server/modules/core/tests/ratelimiter.spec.ts
@@ -1,11 +1,9 @@
 /* istanbul ignore file */
 import { TIME } from '@speckle/shared'
 import {
-  createRateLimiterMiddleware,
   getRateLimitResult,
   isRateLimitBreached,
   getActionForPath,
-  sendRateLimitResponse,
   RateLimitBreached,
   RateLimits,
   createConsumer,
@@ -16,6 +14,10 @@ import {
 import { expect } from 'chai'
 import httpMocks from 'node-mocks-http'
 import { RateLimiterMemory } from 'rate-limiter-flexible'
+import {
+  addRateLimitHeadersToResponse,
+  createRateLimiterMiddleware
+} from '@/modules/core/rest/ratelimiter'
 
 type RateLimiterOptions = {
   [key in RateLimitAction]: RateLimits
@@ -90,7 +92,7 @@ describe('Rate Limiting', () => {
         msBeforeNext: 4900
       }
       const response = httpMocks.createResponse()
-      await sendRateLimitResponse(response, breached)
+      await addRateLimitHeadersToResponse(response, breached)
       assert429response(response)
     })
   })
@@ -139,9 +141,16 @@ describe('Rate Limiting', () => {
       })
 
       let response = httpMocks.createResponse()
-      let nextCalled = 0
-      const next = () => {
-        nextCalled++
+      let nextCalledWithErr = 0
+      let nextCalledWithoutErr = 0
+      const next = (err: unknown) => {
+        if (err) {
+          nextCalledWithErr++
+        } else {
+          nextCalledWithoutErr++
+        }
+        expect(err).to.not.be.undefined
+        expect(err).to.have.property('rateLimitBreached')
       }
 
       const SUT = createRateLimiterMiddleware(createTestRateLimiterMappings())
@@ -151,7 +160,8 @@ describe('Rate Limiting', () => {
         await SUT(request, response, next)
       })
 
-      expect(nextCalled).to.equal(0)
+      expect(nextCalledWithErr).to.equal(1)
+      expect(nextCalledWithoutErr).to.equal(0)
       assert429response(response)
     })
   })
@@ -170,5 +180,5 @@ const assert429response = (response: any) => {
   expect(response.getHeader('X-RateLimit-Remaining')).to.be.undefined
   expect(response.getHeader('Retry-After')).to.be.greaterThanOrEqual(4)
   expect(response.getHeader('X-RateLimit-Reset')).to.not.be.undefined
-  expect(response.statusCode).to.equal(429)
+  // expect(response.statusCode).to.equal(429) // response status code is added by the error handler, which is not part of this integration test
 }
diff --git a/packages/server/modules/gendo/graph/resolvers/index.ts b/packages/server/modules/gendo/graph/resolvers/index.ts
index 86bbc51e5..873420f09 100644
--- a/packages/server/modules/gendo/graph/resolvers/index.ts
+++ b/packages/server/modules/gendo/graph/resolvers/index.ts
@@ -36,7 +36,8 @@ import {
   getGendoAIKey,
   getGendoAICreditLimit,
   getServerOrigin,
-  getFeatureFlags
+  getFeatureFlags,
+  isRateLimiterEnabled
 } from '@/modules/shared/helpers/envHelper'
 import { getProjectObjectStorage } from '@/modules/multiregion/utils/blobStorageSelector'
 import { storeFileStreamFactory } from '@/modules/blobstorage/repositories/blobs'
@@ -86,12 +87,14 @@ export = FF_GENDOAI_MODULE_ENABLED
             ctx.resourceAccessRules
           )
 
-          const rateLimitResult = await getRateLimitResult(
-            'GENDO_AI_RENDER_REQUEST',
-            ctx.userId as string
-          )
-          if (isRateLimitBreached(rateLimitResult)) {
-            throw new RateLimitError(rateLimitResult)
+          if (isRateLimiterEnabled()) {
+            const rateLimitResult = await getRateLimitResult(
+              'GENDO_AI_RENDER_REQUEST',
+              ctx.userId as string
+            )
+            if (isRateLimitBreached(rateLimitResult)) {
+              throw new RateLimitError(rateLimitResult)
+            }
           }
 
           const userId = ctx.userId!
diff --git a/packages/server/modules/shared/helpers/envHelper.ts b/packages/server/modules/shared/helpers/envHelper.ts
index 72602e43b..d145b535c 100644
--- a/packages/server/modules/shared/helpers/envHelper.ts
+++ b/packages/server/modules/shared/helpers/envHelper.ts
@@ -451,3 +451,7 @@ export function enableImprovedKnexTelemetryStackTraces() {
 export function disablePreviews() {
   return getBooleanFromEnv('DISABLE_PREVIEWS')
 }
+
+export const isRateLimiterEnabled = (): boolean => {
+  return getBooleanFromEnv('RATELIMITER_ENABLED', true)
+}
diff --git a/packages/server/modules/workspaces/graph/resolvers/workspaces.ts b/packages/server/modules/workspaces/graph/resolvers/workspaces.ts
index 83b37eef7..2c65ffa5f 100644
--- a/packages/server/modules/workspaces/graph/resolvers/workspaces.ts
+++ b/packages/server/modules/workspaces/graph/resolvers/workspaces.ts
@@ -41,7 +41,11 @@ import {
 import { createProjectInviteFactory } from '@/modules/serverinvites/services/projectInviteManagement'
 import { getInvitationTargetUsersFactory } from '@/modules/serverinvites/services/retrieval'
 import { authorizeResolver } from '@/modules/shared'
-import { getFeatureFlags, getServerOrigin } from '@/modules/shared/helpers/envHelper'
+import {
+  getFeatureFlags,
+  getServerOrigin,
+  isRateLimiterEnabled
+} from '@/modules/shared/helpers/envHelper'
 import { getEventBus } from '@/modules/shared/services/eventBus'
 import { WorkspaceInviteResourceType } from '@/modules/workspacesCore/domain/constants'
 import {
@@ -933,12 +937,14 @@ export = FF_WORKSPACES_MODULE_ENABLED
       },
       WorkspaceProjectMutations: {
         create: async (_parent, args, context) => {
-          const rateLimitResult = await getRateLimitResult(
-            'STREAM_CREATE',
-            context.userId!
-          )
-          if (isRateLimitBreached(rateLimitResult)) {
-            throw new RateLimitError(rateLimitResult)
+          if (isRateLimiterEnabled()) {
+            const rateLimitResult = await getRateLimitResult(
+              'STREAM_CREATE',
+              context.userId!
+            )
+            if (isRateLimitBreached(rateLimitResult)) {
+              throw new RateLimitError(rateLimitResult)
+            }
           }
 
           await authorizeResolver(