diff --git a/.changeset/sixty-lobsters-jump.md b/.changeset/sixty-lobsters-jump.md
new file mode 100644
index 00000000000..e031a69b0ca
--- /dev/null
+++ b/.changeset/sixty-lobsters-jump.md
@@ -0,0 +1,5 @@
+---
+"@clerk/fastify": patch
+---
+
+Add enableHandshake option to plugin
diff --git a/packages/fastify/src/__tests__/withClerkMiddleware.test.ts b/packages/fastify/src/__tests__/withClerkMiddleware.test.ts
index d08316f99ef..03b8c307101 100644
--- a/packages/fastify/src/__tests__/withClerkMiddleware.test.ts
+++ b/packages/fastify/src/__tests__/withClerkMiddleware.test.ts
@@ -142,6 +142,37 @@ describe('withClerkMiddleware(options)', () => {
     });
   });
 
+  test('skips handshake redirect when enableHandshake is false', async () => {
+    authenticateRequestMock.mockResolvedValueOnce({
+      status: 'handshake',
+      headers: new Headers({
+        location: 'https://fapi.example.com/v1/clients/handshake',
+        'x-clerk-auth-status': 'handshake',
+      }),
+      toAuth: () => ({
+        tokenType: 'session_token',
+      }),
+    });
+    const fastify = Fastify();
+    await fastify.register(clerkPlugin, { enableHandshake: false });
+
+    fastify.get('/', (request: FastifyRequest, reply: FastifyReply) => {
+      const auth = getAuth(request);
+      reply.send({ auth });
+    });
+
+    const response = await fastify.inject({
+      method: 'GET',
+      path: '/',
+      headers: {
+        cookie: '__clerk_handshake_nonce=deadbeef; __client_uat=1675692233',
+      },
+    });
+
+    expect(response.statusCode).toEqual(200);
+    expect(response.body).toEqual(JSON.stringify({ auth: { tokenType: 'session_token' } }));
+  });
+
   test('handles signout case by populating the req.auth', async () => {
     authenticateRequestMock.mockResolvedValueOnce({
       headers: new Headers(),
diff --git a/packages/fastify/src/types.ts b/packages/fastify/src/types.ts
index 7b1224ea271..98e50544613 100644
--- a/packages/fastify/src/types.ts
+++ b/packages/fastify/src/types.ts
@@ -21,4 +21,12 @@ export interface FrontendApiProxyOptions {
 export type ClerkFastifyOptions = ClerkOptions & {
   hookName?: (typeof ALLOWED_HOOKS)[number];
   frontendApiProxy?: FrontendApiProxyOptions;
+  /**
+   * Whether to enable the handshake flow for session verification.
+   * Disable this when using Clerk with a first-party API backend (e.g. a SPA calling
+   * a Fastify server) to prevent handshake nonce cookies set during OAuth callbacks
+   * from blocking authentication on subsequent API requests.
+   * @default true
+   */
+  enableHandshake?: boolean;
 };
diff --git a/packages/fastify/src/withClerkMiddleware.ts b/packages/fastify/src/withClerkMiddleware.ts
index bca237ce8d4..1bd50bdb891 100644
--- a/packages/fastify/src/withClerkMiddleware.ts
+++ b/packages/fastify/src/withClerkMiddleware.ts
@@ -11,6 +11,7 @@ import { fastifyRequestToRequest, requestToProxyRequest } from './utils';
 export const withClerkMiddleware = (options: ClerkFastifyOptions) => {
   const frontendApiProxy = options.frontendApiProxy;
   const proxyPath = stripTrailingSlashes(frontendApiProxy?.path ?? DEFAULT_PROXY_PATH) || DEFAULT_PROXY_PATH;
+  const enableHandshake = options.enableHandshake ?? true;
 
   return async (fastifyRequest: FastifyRequest, reply: FastifyReply) => {
     const publishableKey = options.publishableKey || constants.PUBLISHABLE_KEY;
@@ -84,11 +85,13 @@ export const withClerkMiddleware = (options: ClerkFastifyOptions) => {
 
     requestState.headers.forEach((value, key) => reply.header(key, value));
 
-    const locationHeader = requestState.headers.get(constants.Headers.Location);
-    if (locationHeader) {
-      return reply.code(307).send();
-    } else if (requestState.status === AuthStatus.Handshake) {
-      throw new Error('Clerk: handshake status without redirect');
+    if (enableHandshake) {
+      const locationHeader = requestState.headers.get(constants.Headers.Location);
+      if (locationHeader) {
+        return reply.code(307).send();
+      } else if (requestState.status === AuthStatus.Handshake) {
+        throw new Error('Clerk: handshake status without redirect');
+      }
     }
 
     // @ts-expect-error Inject auth so getAuth can read it