diff --git a/.changeset/few-rings-push.md b/.changeset/few-rings-push.md
new file mode 100644
index 00000000000..1e0e56979fc
--- /dev/null
+++ b/.changeset/few-rings-push.md
@@ -0,0 +1,5 @@
+---
+'@clerk/backend': patch
+---
+
+Fix an error in the handshake flow where the request would throw an unhandled error when verification of the handshake payload fails.
diff --git a/integration/tests/handshake.test.ts b/integration/tests/handshake.test.ts
index 23d1926dd8a..b0636403bc2 100644
--- a/integration/tests/handshake.test.ts
+++ b/integration/tests/handshake.test.ts
@@ -827,13 +827,14 @@ test.describe('Client handshake @generic', () => {
       }),
       redirect: 'manual',
     });
-    expect(res.status).toBe(500);
+    expect(res.status).toBe(200);
   });
 
-  test('Handshake result - prod - skew - clock ahead', async () => {
+  test('Handshake result - prod - session token expired and handshake stale', async () => {
     const config = generateConfig({
       mode: 'live',
     });
+    const { token: currentSessionToken, claims } = config.generateToken({ state: 'expired' });
     const { token } = config.generateToken({ state: 'expired' });
     const cookiesToSet = [`__session=${token};path=/`, 'foo=bar;path=/;domain=example.com'];
     const handshake = await config.generateHandshakeToken(cookiesToSet);
@@ -841,12 +842,12 @@ test.describe('Client handshake @generic', () => {
       headers: new Headers({
         'X-Publishable-Key': config.pk,
         'X-Secret-Key': config.sk,
-        Cookie: `__clerk_handshake=${handshake}`,
+        Cookie: `__clerk_handshake=${handshake};__session=${currentSessionToken};__client_uat=${claims.iat}`,
         'Sec-Fetch-Dest': 'document',
       }),
       redirect: 'manual',
     });
-    expect(res.status).toBe(500);
+    expect(res.status).toBe(307);
   });
 
   test('Handshake result - prod - mismatched keys', async () => {
@@ -866,6 +867,6 @@ test.describe('Client handshake @generic', () => {
       }),
       redirect: 'manual',
     });
-    expect(res.status).toBe(500);
+    expect(res.status).toBe(200);
   });
 });
diff --git a/packages/backend/src/tokens/request.ts b/packages/backend/src/tokens/request.ts
index fb383605844..d3d821434d7 100644
--- a/packages/backend/src/tokens/request.ts
+++ b/packages/backend/src/tokens/request.ts
@@ -124,8 +124,8 @@ export async function authenticateRequest(
 
     if (
       instanceType === 'development' &&
-      (error.reason === TokenVerificationErrorReason.TokenExpired ||
-        error.reason === TokenVerificationErrorReason.TokenNotActiveYet)
+      (error?.reason === TokenVerificationErrorReason.TokenExpired ||
+        error?.reason === TokenVerificationErrorReason.TokenNotActiveYet)
     ) {
       error.tokenCarrier = 'cookie';
       // This probably means we're dealing with clock skew
@@ -204,7 +204,21 @@ ${error.getFullMessage()}`,
      * If we have a handshakeToken, resolve the handshake and attempt to return a definitive signed in or signed out state.
      */
     if (authenticateContext.handshakeToken) {
-      return resolveHandshake();
+      try {
+        return await resolveHandshake();
+      } catch (error) {
+        // If for some reason the handshake token is invalid or stale, we ignore it and continue trying to authenticate the request.
+        // Worst case, the handshake will trigger again and return a refreshed token.
+        if (error instanceof TokenVerificationError && instanceType === 'development') {
+          if (error.reason === TokenVerificationErrorReason.TokenInvalidSignature) {
+            throw new Error(
+              `Clerk: Handshake token verification failed due to an invalid signature. If you have switched Clerk keys locally, clear your cookies and try again.`,
+            );
+          }
+
+          throw new Error(`Clerk: Handshake token verification failed: ${error.getFullMessage()}.`);
+        }
+      }
     }
 
     /**