diff --git a/.changeset/five-eagles-tap.md b/.changeset/five-eagles-tap.md
new file mode 100644
index 00000000000..415e5bf8691
--- /dev/null
+++ b/.changeset/five-eagles-tap.md
@@ -0,0 +1,5 @@
+---
+'@clerk/backend': patch
+---
+
+The JWT claims are verified after the signature to avoid leaking information through error messages on forged tokens.
diff --git a/packages/backend/src/jwt/verifyJwt.ts b/packages/backend/src/jwt/verifyJwt.ts
index 3070ddd5d6c..5b828bd8a18 100644
--- a/packages/backend/src/jwt/verifyJwt.ts
+++ b/packages/backend/src/jwt/verifyJwt.ts
@@ -145,20 +145,12 @@ export async function verifyJwt(
 
     assertHeaderType(typ, headerType);
     assertHeaderAlgorithm(alg);
-
-    // Payload verifications
-    const { azp, sub, aud, iat, exp, nbf } = payload;
-
-    assertSubClaim(sub);
-    assertAudienceClaim([aud], [audience]);
-    assertAuthorizedPartiesClaim(azp, authorizedParties);
-    assertExpirationClaim(exp, clockSkew);
-    assertActivationClaim(nbf, clockSkew);
-    assertIssuedAtClaim(iat, clockSkew);
   } catch (err) {
     return { errors: [err as TokenVerificationError] };
   }
 
+  // Verify signature before validating claims to prevent oracle attacks
+  // that could leak configuration details through differential error responses
   const { data: signatureValid, errors: signatureErrors } = await hasValidSignature(decoded, key);
   if (signatureErrors) {
     return {
@@ -183,5 +175,19 @@ export async function verifyJwt(
     };
   }
 
+  // Payload verifications (only after signature is confirmed valid)
+  try {
+    const { azp, sub, aud, iat, exp, nbf } = payload;
+
+    assertSubClaim(sub);
+    assertAudienceClaim([aud], [audience]);
+    assertAuthorizedPartiesClaim(azp, authorizedParties);
+    assertExpirationClaim(exp, clockSkew);
+    assertActivationClaim(nbf, clockSkew);
+    assertIssuedAtClaim(iat, clockSkew);
+  } catch (err) {
+    return { errors: [err as TokenVerificationError] };
+  }
+
   return { data: payload };
 }
diff --git a/packages/backend/src/tokens/__tests__/request.test.ts b/packages/backend/src/tokens/__tests__/request.test.ts
index b9cc1d67f68..e9b5fa6bfda 100644
--- a/packages/backend/src/tokens/__tests__/request.test.ts
+++ b/packages/backend/src/tokens/__tests__/request.test.ts
@@ -8,7 +8,7 @@ import {
   mockJwks,
   mockJwt,
   mockJwtPayload,
-  mockMalformedJwt,
+  signingJwks,
 } from '../../fixtures';
 import {
   mockMachineAuthResponses,
@@ -16,6 +16,7 @@ import {
   mockTokens,
   mockVerificationResults,
 } from '../../fixtures/machine';
+import { signJwt } from '../../jwt/signJwt';
 import { server } from '../../mock-server';
 import type { AuthReason } from '../authStatus';
 import { AuthErrorReason, AuthStatus } from '../authStatus';
@@ -1193,13 +1194,20 @@ describe('tokens.authenticateRequest(options)', () => {
       }),
     );
 
+    // Create a properly signed JWT that is missing the 'sub' claim
+    const { sub: _, ...payloadWithoutSub } = mockJwtPayload;
+    const { data: malformedJwt } = await signJwt(payloadWithoutSub, signingJwks, {
+      algorithm: 'RS256',
+      header: { typ: 'JWT', kid: 'ins_2GIoQhbUpy0hX7B2cVkuTMinXoD' },
+    });
+
     const requestState = await authenticateRequest(
       mockRequestWithCookies(
         {},
         {
           __clerk_db_jwt: 'deadbeef',
           __client_uat: `${mockJwtPayload.iat - 10}`,
-          __session: mockMalformedJwt,
+          __session: malformedJwt!,
         },
       ),
       mockOptions(),
diff --git a/packages/backend/src/tokens/__tests__/verify.test.ts b/packages/backend/src/tokens/__tests__/verify.test.ts
index b682db6ef37..a396d796504 100644
--- a/packages/backend/src/tokens/__tests__/verify.test.ts
+++ b/packages/backend/src/tokens/__tests__/verify.test.ts
@@ -20,14 +20,15 @@ import { signJwt } from '../../jwt/signJwt';
 import { server, validateHeaders } from '../../mock-server';
 import { verifyMachineAuthToken, verifyToken } from '../verify';
 
-function createOAuthJwt(
+async function createSignedOAuthJwt(
   payload = mockOAuthAccessTokenJwtPayload,
   typ: 'at+jwt' | 'application/at+jwt' | 'JWT' = 'at+jwt',
 ) {
-  return createJwt({
+  const { data } = await signJwt(payload, signingJwks, {
+    algorithm: 'RS256',
     header: { typ, kid: 'ins_2GIoQhbUpy0hX7B2cVkuTMinXoD' },
-    payload,
   });
+  return data!;
 }
 
 async function createSignedM2MJwt(payload = mockM2MJwtPayload) {
@@ -85,6 +86,32 @@ describe('tokens.verify(token, options)', () => {
 
     expect(data).toEqual(mockJwtPayload);
   });
+
+  it('returns signature error before claims error when both are invalid', async () => {
+    server.use(
+      http.get(
+        'https://api.clerk.test/v1/jwks',
+        validateHeaders(() => {
+          return HttpResponse.json(mockJwks);
+        }),
+      ),
+    );
+
+    // Create a JWT with expired claims AND an invalid signature
+    const expiredJwt = createJwt({
+      payload: { ...mockJwtPayload, exp: mockJwtPayload.iat - 100 },
+    });
+
+    const { errors } = await verifyToken(expiredJwt, {
+      apiUrl: 'https://api.clerk.test',
+      secretKey: 'a-valid-key',
+      authorizedParties: ['https://accounts.inspired.puma-74.lcl.dev'],
+      skipJwksCache: true,
+    });
+
+    expect(errors).toBeDefined();
+    expect(errors?.[0].message).toContain('signature');
+  });
 });
 
 describe('tokens.verifyMachineAuthToken(token, options)', () => {
@@ -392,7 +419,7 @@ describe('tokens.verifyMachineAuthToken(token, options)', () => {
         ),
       );
 
-      const oauthJwt = createOAuthJwt(mockOAuthAccessTokenJwtPayload, 'JWT');
+      const oauthJwt = await createSignedOAuthJwt(mockOAuthAccessTokenJwtPayload, 'JWT');
 
       const result = await verifyMachineAuthToken(oauthJwt, {
         apiUrl: 'https://api.clerk.test',
@@ -472,7 +499,7 @@ describe('tokens.verifyMachineAuthToken(token, options)', () => {
         exp: mockOAuthAccessTokenJwtPayload.iat - 100,
       };
 
-      const oauthJwt = createOAuthJwt(expiredPayload, 'at+jwt');
+      const oauthJwt = await createSignedOAuthJwt(expiredPayload);
 
       const result = await verifyMachineAuthToken(oauthJwt, {
         apiUrl: 'https://api.clerk.test',