diff --git a/e2e/react-start/server-functions/src/routeTree.gen.ts b/e2e/react-start/server-functions/src/routeTree.gen.ts
index 51327cb8164..34595c339d0 100644
--- a/e2e/react-start/server-functions/src/routeTree.gen.ts
+++ b/e2e/react-start/server-functions/src/routeTree.gen.ts
@@ -35,6 +35,8 @@ import { Route as RedirectTestSsrTargetRouteImport } from './routes/redirect-tes
 import { Route as MiddlewareSendServerFnRouteImport } from './routes/middleware/send-serverFn'
 import { Route as MiddlewareRequestMiddlewareRouteImport } from './routes/middleware/request-middleware'
 import { Route as MiddlewareClientMiddlewareRouterRouteImport } from './routes/middleware/client-middleware-router'
+import { Route as MethodNotAllowedPostRouteImport } from './routes/method-not-allowed/post'
+import { Route as MethodNotAllowedGetRouteImport } from './routes/method-not-allowed/get'
 import { Route as CookiesSetRouteImport } from './routes/cookies/set'
 import { Route as FormdataRedirectTargetNameRouteImport } from './routes/formdata-redirect/target.$name'
 
@@ -170,6 +172,16 @@ const MiddlewareClientMiddlewareRouterRoute =
     path: '/middleware/client-middleware-router',
     getParentRoute: () => rootRouteImport,
   } as any)
+const MethodNotAllowedPostRoute = MethodNotAllowedPostRouteImport.update({
+  id: '/method-not-allowed/post',
+  path: '/method-not-allowed/post',
+  getParentRoute: () => rootRouteImport,
+} as any)
+const MethodNotAllowedGetRoute = MethodNotAllowedGetRouteImport.update({
+  id: '/method-not-allowed/get',
+  path: '/method-not-allowed/get',
+  getParentRoute: () => rootRouteImport,
+} as any)
 const CookiesSetRoute = CookiesSetRouteImport.update({
   id: '/cookies/set',
   path: '/cookies/set',
@@ -198,6 +210,8 @@ export interface FileRoutesByFullPath {
   '/status': typeof StatusRoute
   '/submit-post-formdata': typeof SubmitPostFormdataRoute
   '/cookies/set': typeof CookiesSetRoute
+  '/method-not-allowed/get': typeof MethodNotAllowedGetRoute
+  '/method-not-allowed/post': typeof MethodNotAllowedPostRoute
   '/middleware/client-middleware-router': typeof MiddlewareClientMiddlewareRouterRoute
   '/middleware/request-middleware': typeof MiddlewareRequestMiddlewareRoute
   '/middleware/send-serverFn': typeof MiddlewareSendServerFnRoute
@@ -228,6 +242,8 @@ export interface FileRoutesByTo {
   '/status': typeof StatusRoute
   '/submit-post-formdata': typeof SubmitPostFormdataRoute
   '/cookies/set': typeof CookiesSetRoute
+  '/method-not-allowed/get': typeof MethodNotAllowedGetRoute
+  '/method-not-allowed/post': typeof MethodNotAllowedPostRoute
   '/middleware/client-middleware-router': typeof MiddlewareClientMiddlewareRouterRoute
   '/middleware/request-middleware': typeof MiddlewareRequestMiddlewareRoute
   '/middleware/send-serverFn': typeof MiddlewareSendServerFnRoute
@@ -259,6 +275,8 @@ export interface FileRoutesById {
   '/status': typeof StatusRoute
   '/submit-post-formdata': typeof SubmitPostFormdataRoute
   '/cookies/set': typeof CookiesSetRoute
+  '/method-not-allowed/get': typeof MethodNotAllowedGetRoute
+  '/method-not-allowed/post': typeof MethodNotAllowedPostRoute
   '/middleware/client-middleware-router': typeof MiddlewareClientMiddlewareRouterRoute
   '/middleware/request-middleware': typeof MiddlewareRequestMiddlewareRoute
   '/middleware/send-serverFn': typeof MiddlewareSendServerFnRoute
@@ -291,6 +309,8 @@ export interface FileRouteTypes {
     | '/status'
     | '/submit-post-formdata'
     | '/cookies/set'
+    | '/method-not-allowed/get'
+    | '/method-not-allowed/post'
     | '/middleware/client-middleware-router'
     | '/middleware/request-middleware'
     | '/middleware/send-serverFn'
@@ -321,6 +341,8 @@ export interface FileRouteTypes {
     | '/status'
     | '/submit-post-formdata'
     | '/cookies/set'
+    | '/method-not-allowed/get'
+    | '/method-not-allowed/post'
     | '/middleware/client-middleware-router'
     | '/middleware/request-middleware'
     | '/middleware/send-serverFn'
@@ -351,6 +373,8 @@ export interface FileRouteTypes {
     | '/status'
     | '/submit-post-formdata'
     | '/cookies/set'
+    | '/method-not-allowed/get'
+    | '/method-not-allowed/post'
     | '/middleware/client-middleware-router'
     | '/middleware/request-middleware'
     | '/middleware/send-serverFn'
@@ -382,6 +406,8 @@ export interface RootRouteChildren {
   StatusRoute: typeof StatusRoute
   SubmitPostFormdataRoute: typeof SubmitPostFormdataRoute
   CookiesSetRoute: typeof CookiesSetRoute
+  MethodNotAllowedGetRoute: typeof MethodNotAllowedGetRoute
+  MethodNotAllowedPostRoute: typeof MethodNotAllowedPostRoute
   MiddlewareClientMiddlewareRouterRoute: typeof MiddlewareClientMiddlewareRouterRoute
   MiddlewareRequestMiddlewareRoute: typeof MiddlewareRequestMiddlewareRoute
   MiddlewareSendServerFnRoute: typeof MiddlewareSendServerFnRoute
@@ -581,6 +607,20 @@ declare module '@tanstack/react-router' {
       preLoaderRoute: typeof MiddlewareClientMiddlewareRouterRouteImport
       parentRoute: typeof rootRouteImport
     }
+    '/method-not-allowed/post': {
+      id: '/method-not-allowed/post'
+      path: '/method-not-allowed/post'
+      fullPath: '/method-not-allowed/post'
+      preLoaderRoute: typeof MethodNotAllowedPostRouteImport
+      parentRoute: typeof rootRouteImport
+    }
+    '/method-not-allowed/get': {
+      id: '/method-not-allowed/get'
+      path: '/method-not-allowed/get'
+      fullPath: '/method-not-allowed/get'
+      preLoaderRoute: typeof MethodNotAllowedGetRouteImport
+      parentRoute: typeof rootRouteImport
+    }
     '/cookies/set': {
       id: '/cookies/set'
       path: '/cookies/set'
@@ -614,6 +654,8 @@ const rootRouteChildren: RootRouteChildren = {
   StatusRoute: StatusRoute,
   SubmitPostFormdataRoute: SubmitPostFormdataRoute,
   CookiesSetRoute: CookiesSetRoute,
+  MethodNotAllowedGetRoute: MethodNotAllowedGetRoute,
+  MethodNotAllowedPostRoute: MethodNotAllowedPostRoute,
   MiddlewareClientMiddlewareRouterRoute: MiddlewareClientMiddlewareRouterRoute,
   MiddlewareRequestMiddlewareRoute: MiddlewareRequestMiddlewareRoute,
   MiddlewareSendServerFnRoute: MiddlewareSendServerFnRoute,
diff --git a/e2e/react-start/server-functions/src/routes/method-not-allowed/get.tsx b/e2e/react-start/server-functions/src/routes/method-not-allowed/get.tsx
new file mode 100644
index 00000000000..c07679ee475
--- /dev/null
+++ b/e2e/react-start/server-functions/src/routes/method-not-allowed/get.tsx
@@ -0,0 +1,56 @@
+import { createFileRoute } from '@tanstack/react-router'
+import { createServerFn } from '@tanstack/react-start'
+import { useState } from 'react'
+
+export const Route = createFileRoute('/method-not-allowed/get')({
+  component: MethodNotAllowedFn,
+})
+
+export const getableServerFn = createServerFn({ method: 'GET' }).handler(() => {
+  return new Response('Hello, World!')
+})
+
+const fetchFn = async (method: string) => {
+  const response = await fetch('/_serverFn/constant_id_2?createServerFn', {
+    method,
+  })
+  return [response.status, await response.text()] as const
+}
+
+function MethodNotAllowedFn() {
+  const [fetchResult, setFetchResult] = useState<
+    readonly [number, string] | null
+  >(null)
+  return (
+    <div className="flex flex-col gap-2">
+      <h1>Method Not Allowed GET</h1>
+
+      <button
+        data-testid="get-button"
+        onClick={() => fetchFn('GET').then(setFetchResult)}
+      >
+        Fetch GET
+      </button>
+      <button
+        data-testid="post-button"
+        onClick={() => fetchFn('POST').then(setFetchResult)}
+      >
+        Fetch POST
+      </button>
+      <button
+        data-testid="put-button"
+        onClick={() => fetchFn('PUT').then(setFetchResult)}
+      >
+        Fetch PUT
+      </button>
+      <button
+        data-testid="options-button"
+        onClick={() => fetchFn('OPTIONS').then(setFetchResult)}
+      >
+        Fetch OPTIONS
+      </button>
+
+      <pre data-testid="fetch-result">{JSON.stringify(fetchResult)}</pre>
+    </div>
+  )
+}
diff --git a/e2e/react-start/server-functions/src/routes/method-not-allowed/post.tsx b/e2e/react-start/server-functions/src/routes/method-not-allowed/post.tsx
new file mode 100644
index 00000000000..e25a4b588b5
--- /dev/null
+++ b/e2e/react-start/server-functions/src/routes/method-not-allowed/post.tsx
@@ -0,0 +1,58 @@
+import { createFileRoute } from '@tanstack/react-router'
+import { createServerFn } from '@tanstack/react-start'
+import { useState } from 'react'
+
+export const Route = createFileRoute('/method-not-allowed/post')({
+  component: MethodNotAllowedFn,
+})
+
+export const postableServerFn = createServerFn({ method: 'POST' }).handler(
+  () => {
+    return new Response('Hello, World!')
+  },
+)
+
+const fetchFn = async (method: string) => {
+  const response = await fetch('/_serverFn/constant_id_3?createServerFn', {
+    method,
+  })
+  return [response.status, await response.text()] as const
+}
+
+function MethodNotAllowedFn() {
+  const [fetchResult, setFetchResult] = useState<
+    readonly [number, string] | null
+  >(null)
+  return (
+    <div className="flex flex-col gap-2">
+      <h1>Method Not Allowed POST</h1>
+
+      <button
+        data-testid="get-button"
+        onClick={() => fetchFn('GET').then(setFetchResult)}
+      >
+        Fetch GET
+      </button>
+      <button
+        data-testid="post-button"
+        onClick={() => fetchFn('POST').then(setFetchResult)}
+      >
+        Fetch POST
+      </button>
+      <button
+        data-testid="put-button"
+        onClick={() => fetchFn('PUT').then(setFetchResult)}
+      >
+        Fetch PUT
+      </button>
+      <button
+        data-testid="options-button"
+        onClick={() => fetchFn('OPTIONS').then(setFetchResult)}
+      >
+        Fetch OPTIONS
+      </button>
+
+      <pre data-testid="fetch-result">{JSON.stringify(fetchResult)}</pre>
+    </div>
+  )
+}
diff --git a/e2e/react-start/server-functions/tests/server-functions.spec.ts b/e2e/react-start/server-functions/tests/server-functions.spec.ts
index b384be2ea6f..8b2f2cedc5d 100644
--- a/e2e/react-start/server-functions/tests/server-functions.spec.ts
+++ b/e2e/react-start/server-functions/tests/server-functions.spec.ts
@@ -541,3 +541,65 @@ test('redirect in server function called in query during SSR', async ({
   await expect(page.getByTestId('redirect-target-ssr')).toBeVisible()
   expect(page.url()).toContain('/redirect-test-ssr/target')
 })
+
+test.describe('server function returns 405 when method is not allowed', () => {
+  test('serverFn defined with GET method', async ({ page }) => {
+    await page.goto('/method-not-allowed/get')
+
+    await page.waitForLoadState('networkidle')
+
+    await page.getByTestId('get-button').click()
+    await page.waitForLoadState('networkidle')
+    await expect(page.getByTestId('fetch-result')).toContainText(
+      '[200,"Hello, World!"]',
+    )
+
+    await page.getByTestId('post-button').click()
+    await page.waitForLoadState('networkidle')
+    await expect(page.getByTestId('fetch-result')).toContainText(
+      '[405,"expected GET method. Got POST"]',
+    )
+
+    await page.getByTestId('put-button').click()
+    await page.waitForLoadState('networkidle')
+    await expect(page.getByTestId('fetch-result')).toContainText(
+      '[405,"expected GET method. Got PUT"]',
+    )
+
+    await page.getByTestId('options-button').click()
+    await page.waitForLoadState('networkidle')
+    await expect(page.getByTestId('fetch-result')).toContainText(
+      '[405,"expected GET method. Got OPTIONS"]',
+    )
+  })
+
+  test('serverFn defined with POST method', async ({ page }) => {
+    await page.goto('/method-not-allowed/post')
+
+    await page.waitForLoadState('networkidle')
+
+    await page.getByTestId('get-button').click()
+    await page.waitForLoadState('networkidle')
+    await expect(page.getByTestId('fetch-result')).toContainText(
+      '[405,"expected POST method. Got GET"]',
+    )
+
+    await page.getByTestId('post-button').click()
+    await page.waitForLoadState('networkidle')
+    await expect(page.getByTestId('fetch-result')).toContainText(
+      '[200,"Hello, World!"]',
+    )
+
+    await page.getByTestId('put-button').click()
+    await page.waitForLoadState('networkidle')
+    await expect(page.getByTestId('fetch-result')).toContainText(
+      '[405,"expected POST method. Got PUT"]',
+    )
+
+    await page.getByTestId('options-button').click()
+    await page.waitForLoadState('networkidle')
+    await expect(page.getByTestId('fetch-result')).toContainText(
+      '[405,"expected POST method. Got OPTIONS"]',
+    )
+  })
+})
diff --git a/e2e/react-start/server-functions/vite.config.ts b/e2e/react-start/server-functions/vite.config.ts
index 97ff657630e..3df377bbd3f 100644
--- a/e2e/react-start/server-functions/vite.config.ts
+++ b/e2e/react-start/server-functions/vite.config.ts
@@ -6,6 +6,8 @@ import viteReact from '@vitejs/plugin-react'
 const FUNCTIONS_WITH_CONSTANT_ID = [
   'src/routes/submit-post-formdata.tsx/greetUser_createServerFn_handler',
   'src/routes/formdata-redirect/index.tsx/greetUser_createServerFn_handler',
+  'src/routes/method-not-allowed/get.tsx/getableServerFn_createServerFn_handler',
+  'src/routes/method-not-allowed/post.tsx/postableServerFn_createServerFn_handler',
 ]
 
 export default defineConfig({
diff --git a/packages/start-server-core/src/server-functions-handler.ts b/packages/start-server-core/src/server-functions-handler.ts
index 69e0dc19bc4..b9f8b82f34b 100644
--- a/packages/start-server-core/src/server-functions-handler.ts
+++ b/packages/start-server-core/src/server-functions-handler.ts
@@ -12,6 +12,15 @@ import { getServerFnById } from './getServerFnById'
 
 let regex: RegExp | undefined = undefined
 
+const methodNotAllowed = (expectedMethod: string, actualMethod: string) => {
+  throw new Response(`expected ${expectedMethod} method. Got ${actualMethod}`, {
+    status: 405,
+    headers: {
+      Allow: expectedMethod,
+    },
+  })
+}
+
 export const handleServerAction = async ({
   request,
   context,
@@ -119,7 +128,7 @@ export const handleServerAction = async ({
         }
 
         if (method.toLowerCase() !== 'post') {
-          throw new Error('expected POST method')
+          throw methodNotAllowed('POST', method)
         }
 
         let jsonPayload