diff --git a/packages/backend/src/tokens/__tests__/authenticateContext.test.ts b/packages/backend/src/tokens/__tests__/authenticateContext.test.ts
index 10b4a02bf62..dfaa350820e 100644
--- a/packages/backend/src/tokens/__tests__/authenticateContext.test.ts
+++ b/packages/backend/src/tokens/__tests__/authenticateContext.test.ts
@@ -214,6 +214,46 @@ describe('AuthenticateContext', () => {
     });
   });
 
+  describe('auto-proxy for .vercel.app', () => {
+    it('auto-derives proxyUrl for .vercel.app hostnames', async () => {
+      const clerkRequest = createClerkRequest(new Request('https://myapp-abc123.vercel.app/dashboard'));
+      const context = await createAuthenticateContext(clerkRequest, {
+        publishableKey: pkTest,
+      });
+
+      expect(context.proxyUrl).toBe('https://myapp-abc123.vercel.app/__clerk');
+    });
+
+    it('does NOT auto-derive proxyUrl for non-.vercel.app domains', async () => {
+      const clerkRequest = createClerkRequest(new Request('https://myapp.com/dashboard'));
+      const context = await createAuthenticateContext(clerkRequest, {
+        publishableKey: pkTest,
+      });
+
+      expect(context.proxyUrl).toBeUndefined();
+    });
+
+    it('explicit proxyUrl takes precedence over auto-detection', async () => {
+      const clerkRequest = createClerkRequest(new Request('https://myapp-abc123.vercel.app/dashboard'));
+      const context = await createAuthenticateContext(clerkRequest, {
+        publishableKey: pkTest,
+        proxyUrl: 'https://custom-proxy.example.com/__clerk',
+      });
+
+      expect(context.proxyUrl).toBe('https://custom-proxy.example.com/__clerk');
+    });
+
+    it('explicit domain skips auto-detection', async () => {
+      const clerkRequest = createClerkRequest(new Request('https://myapp-abc123.vercel.app/dashboard'));
+      const context = await createAuthenticateContext(clerkRequest, {
+        publishableKey: pkTest,
+        domain: 'clerk.myapp.com',
+      });
+
+      expect(context.proxyUrl).toBeUndefined();
+    });
+  });
+
   // Added these tests to verify that the generated sha-1 is the same as the one used in cookie assignment
   // Tests copied from packages/shared/src/__tests__/keys.test.ts
   describe('getCookieSuffix(publishableKey, subtle)', () => {
diff --git a/packages/backend/src/tokens/authenticateContext.ts b/packages/backend/src/tokens/authenticateContext.ts
index 6d9fdcb9c5a..9b91c8e0d45 100644
--- a/packages/backend/src/tokens/authenticateContext.ts
+++ b/packages/backend/src/tokens/authenticateContext.ts
@@ -1,4 +1,5 @@
 import { buildAccountsBaseUrl } from '@clerk/shared/buildAccountsBaseUrl';
+import { isVercelPreviewDeploy } from '@clerk/shared/proxy';
 import type { Jwt } from '@clerk/shared/types';
 import { isCurrentDevAccountPortalOrigin, isLegacyDevAccountPortalOrigin } from '@clerk/shared/url';
 
@@ -69,6 +70,14 @@ class AuthenticateContext implements AuthenticateContext {
     private clerkRequest: ClerkRequest,
     options: AuthenticateRequestOptions,
   ) {
+    // Auto-detect proxy for Vercel preview deployments
+    if (!options.proxyUrl && !options.domain) {
+      const hostname = clerkRequest.clerkUrl.hostname;
+      if (isVercelPreviewDeploy(hostname)) {
+        options = { ...options, proxyUrl: `${clerkRequest.clerkUrl.origin}/__clerk` };
+      }
+    }
+
     if (options.acceptsToken === TokenType.M2MToken || options.acceptsToken === TokenType.ApiKey) {
       // For non-session tokens, we only want to set the header values.
       this.initHeaderValues();
diff --git a/packages/clerk-js/src/core/__tests__/clerk.test.ts b/packages/clerk-js/src/core/__tests__/clerk.test.ts
index 4d9fb15bc5b..41f7b6224d2 100644
--- a/packages/clerk-js/src/core/__tests__/clerk.test.ts
+++ b/packages/clerk-js/src/core/__tests__/clerk.test.ts
@@ -2491,6 +2491,71 @@ describe('Clerk singleton', () => {
         expect(sut.getFapiClient().buildUrl({ path: '/me' }).href).toContain('https://proxy.com/api/__clerk/v1/me');
       });
     });
+
+    describe('auto-detection for .vercel.app', () => {
+      const originalLocation = window.location;
+
+      afterEach(() => {
+        Object.defineProperty(window, 'location', {
+          value: originalLocation,
+          writable: true,
+        });
+      });
+
+      test('auto-derives proxyUrl when hostname is .vercel.app', () => {
+        Object.defineProperty(window, 'location', {
+          value: {
+            ...originalLocation,
+            hostname: 'myapp-abc123.vercel.app',
+            origin: 'https://myapp-abc123.vercel.app',
+            href: 'https://myapp-abc123.vercel.app/dashboard',
+          },
+          writable: true,
+        });
+
+        const sut = new Clerk(developmentPublishableKey);
+        expect(sut.proxyUrl).toBe('https://myapp-abc123.vercel.app/__clerk');
+      });
+
+      test('does NOT auto-derive proxyUrl for non-.vercel.app domains', () => {
+        const sut = new Clerk(developmentPublishableKey);
+        expect(sut.proxyUrl).toBe('');
+      });
+
+      test('explicit proxyUrl takes precedence over auto-detection', () => {
+        Object.defineProperty(window, 'location', {
+          value: {
+            ...originalLocation,
+            hostname: 'myapp-abc123.vercel.app',
+            origin: 'https://myapp-abc123.vercel.app',
+            href: 'https://myapp-abc123.vercel.app/dashboard',
+          },
+          writable: true,
+        });
+
+        const sut = new Clerk(developmentPublishableKey, {
+          proxyUrl: 'https://custom-proxy.example.com/__clerk',
+        });
+        expect(sut.proxyUrl).toBe('https://custom-proxy.example.com/__clerk');
+      });
+
+      test('explicit domain skips auto-detection', () => {
+        Object.defineProperty(window, 'location', {
+          value: {
+            ...originalLocation,
+            hostname: 'myapp-abc123.vercel.app',
+            origin: 'https://myapp-abc123.vercel.app',
+            href: 'https://myapp-abc123.vercel.app/dashboard',
+          },
+          writable: true,
+        });
+
+        const sut = new Clerk(developmentPublishableKey, {
+          domain: 'clerk.myapp.com',
+        });
+        expect(sut.proxyUrl).toBe('');
+      });
+    });
   });
 
   describe('buildUrlWithAuth', () => {
diff --git a/packages/clerk-js/src/core/clerk.ts b/packages/clerk-js/src/core/clerk.ts
index b6ac5321a41..8a8f21c4b25 100644
--- a/packages/clerk-js/src/core/clerk.ts
+++ b/packages/clerk-js/src/core/clerk.ts
@@ -37,7 +37,7 @@ import { windowNavigate } from '@clerk/shared/internal/clerk-js/windowNavigate';
 import { parsePublishableKey } from '@clerk/shared/keys';
 import { logger } from '@clerk/shared/logger';
 import { CLERK_NETLIFY_CACHE_BUST_PARAM } from '@clerk/shared/netlifyCacheHandler';
-import { isHttpOrHttps, isValidProxyUrl, proxyUrlToAbsoluteURL } from '@clerk/shared/proxy';
+import { isHttpOrHttps, isValidProxyUrl, isVercelPreviewDeploy, proxyUrlToAbsoluteURL } from '@clerk/shared/proxy';
 import {
   eventPrebuiltComponentMounted,
   eventPrebuiltComponentOpened,
@@ -350,7 +350,14 @@ export class Clerk implements ClerkInterface {
       if (!isValidProxyUrl(_unfilteredProxy)) {
         errorThrower.throwInvalidProxyUrl({ url: _unfilteredProxy });
       }
-      return proxyUrlToAbsoluteURL(_unfilteredProxy);
+      const resolved = proxyUrlToAbsoluteURL(_unfilteredProxy);
+      if (resolved) {
+        return resolved;
+      }
+      // Auto-detect for Vercel preview deployments when no explicit proxy or domain is configured
+      if (!this.#domain && isVercelPreviewDeploy(window.location.hostname)) {
+        return `${window.location.origin}/__clerk`;
+      }
     }
     return '';
   }
diff --git a/packages/nextjs/src/server/__tests__/clerkMiddleware.test.ts b/packages/nextjs/src/server/__tests__/clerkMiddleware.test.ts
index 101589ae596..ba4ce124360 100644
--- a/packages/nextjs/src/server/__tests__/clerkMiddleware.test.ts
+++ b/packages/nextjs/src/server/__tests__/clerkMiddleware.test.ts
@@ -1191,6 +1191,21 @@ describe('frontendApiProxy multi-domain support', () => {
   });
 });
 
+describe('auto-proxy for .vercel.app', () => {
+  it('auto-intercepts /__clerk/* requests on .vercel.app hostnames', async () => {
+    const req = new NextRequest(new URL('/__clerk/v1/client', 'https://myapp-abc123.vercel.app').toString(), {
+      method: 'GET',
+      headers: new Headers(),
+    });
+
+    const resp = await clerkMiddleware()(req, {} as NextFetchEvent);
+
+    // Proxy should intercept the request — authenticateRequest should NOT be called
+    expect((await clerkClient()).authenticateRequest).not.toBeCalled();
+    expect(resp?.status).toBeDefined();
+  });
+});
+
 describe('contentSecurityPolicy option', () => {
   it('forwards CSP headers as request headers when strict mode is enabled', async () => {
     const resp = await clerkMiddleware({
diff --git a/packages/nextjs/src/server/clerkMiddleware.ts b/packages/nextjs/src/server/clerkMiddleware.ts
index c50949ef99f..bdb1e592b72 100644
--- a/packages/nextjs/src/server/clerkMiddleware.ts
+++ b/packages/nextjs/src/server/clerkMiddleware.ts
@@ -23,6 +23,7 @@ import {
 import { clerkFrontendApiProxy, DEFAULT_PROXY_PATH, matchProxyPath } from '@clerk/backend/proxy';
 import { parsePublishableKey } from '@clerk/shared/keys';
 import { handleNetlifyCacheInDevInstance } from '@clerk/shared/netlifyCacheHandler';
+import { isVercelPreviewDeploy } from '@clerk/shared/proxy';
 import { notFound as nextjsNotFound } from 'next/navigation';
 import type { NextMiddleware, NextRequest } from 'next/server';
 import { NextResponse } from 'next/server';
@@ -33,7 +34,7 @@ import { isRedirect, serverRedirectWithAuth, setHeader } from '../utils';
 import { withLogger } from '../utils/debugLogger';
 import { canUseKeyless } from '../utils/feature-flags';
 import { clerkClient } from './clerkClient';
-import { PUBLISHABLE_KEY, SECRET_KEY, SIGN_IN_URL, SIGN_UP_URL } from './constants';
+import { DOMAIN, PROXY_URL, PUBLISHABLE_KEY, SECRET_KEY, SIGN_IN_URL, SIGN_UP_URL } from './constants';
 import { type ContentSecurityPolicyOptions, createContentSecurityPolicyHeaders } from './content-security-policy';
 import { errorThrower } from './errorThrower';
 import { getHeader } from './headers-utils';
@@ -159,12 +160,16 @@ export const clerkMiddleware = ((...args: unknown[]): NextMiddleware | NextMiddl
       );
 
       // Handle Frontend API proxy requests early, before authentication
-      const frontendApiProxyConfig = resolvedParams.frontendApiProxy;
+      const requestUrl = new URL(request.url);
+      const frontendApiProxyConfig =
+        resolvedParams.frontendApiProxy ??
+        (resolvedParams.proxyUrl || PROXY_URL || resolvedParams.domain || DOMAIN
+          ? undefined
+          : getAutoDetectedProxyConfig(requestUrl));
       if (frontendApiProxyConfig) {
         const { enabled, path: proxyPath = DEFAULT_PROXY_PATH } = frontendApiProxyConfig;
 
         // Resolve enabled - either boolean or function
-        const requestUrl = new URL(request.url);
         const isEnabled = typeof enabled === 'function' ? enabled(requestUrl) : enabled;
 
         if (isEnabled && matchProxyPath(request, { proxyPath })) {
@@ -576,3 +581,10 @@ const handleControlFlowErrors = (
 
   throw e;
 };
+
+function getAutoDetectedProxyConfig(requestUrl: URL): FrontendApiProxyOptions | undefined {
+  if (isVercelPreviewDeploy(requestUrl.hostname)) {
+    return { enabled: true };
+  }
+  return undefined;
+}
diff --git a/packages/shared/src/__tests__/proxy.spec.ts b/packages/shared/src/__tests__/proxy.spec.ts
index 4a898391ee6..4ac55fb692b 100644
--- a/packages/shared/src/__tests__/proxy.spec.ts
+++ b/packages/shared/src/__tests__/proxy.spec.ts
@@ -1,6 +1,12 @@
 import { afterEach, beforeEach, describe, expect, it } from 'vitest';
 
-import { isHttpOrHttps, isProxyUrlRelative, isValidProxyUrl, proxyUrlToAbsoluteURL } from '../proxy';
+import {
+  isHttpOrHttps,
+  isProxyUrlRelative,
+  isValidProxyUrl,
+  isVercelPreviewDeploy,
+  proxyUrlToAbsoluteURL,
+} from '../proxy';
 
 describe('isValidProxyUrl(key)', () => {
   it('returns true if the proxyUrl is valid', () => {
@@ -38,6 +44,28 @@ describe('isHttpOrHttps(key)', () => {
   });
 });
 
+describe('isVercelPreviewDeploy(hostname)', () => {
+  it('returns true for a .vercel.app subdomain', () => {
+    expect(isVercelPreviewDeploy('myapp.vercel.app')).toBe(true);
+  });
+
+  it('returns true for a git branch preview subdomain', () => {
+    expect(isVercelPreviewDeploy('myapp-git-branch.vercel.app')).toBe(true);
+  });
+
+  it('returns false for the bare vercel.app domain', () => {
+    expect(isVercelPreviewDeploy('vercel.app')).toBe(false);
+  });
+
+  it('returns false for a custom domain', () => {
+    expect(isVercelPreviewDeploy('myapp.com')).toBe(false);
+  });
+
+  it('returns false for a domain that contains vercel.app but is not a subdomain', () => {
+    expect(isVercelPreviewDeploy('vercel.app.evil.com')).toBe(false);
+  });
+});
+
 describe('proxyUrlToAbsoluteURL(url)', () => {
   const currentLocation = global.window.location;
 
diff --git a/packages/shared/src/proxy.ts b/packages/shared/src/proxy.ts
index f7633ed1773..b4765a76ff8 100644
--- a/packages/shared/src/proxy.ts
+++ b/packages/shared/src/proxy.ts
@@ -33,6 +33,10 @@ export function proxyUrlToAbsoluteURL(url: string | undefined): string {
   return isProxyUrlRelative(url) ? new URL(url, window.location.origin).toString() : url;
 }
 
+export function isVercelPreviewDeploy(hostname: string): boolean {
+  return hostname.endsWith('.vercel.app');
+}
+
 /**
  * Function that determines whether proxy should be used for a given URL.
  */