diff --git a/.changeset/lucky-pigs-look.md b/.changeset/lucky-pigs-look.md
new file mode 100644
index 00000000000..9705ee128b9
--- /dev/null
+++ b/.changeset/lucky-pigs-look.md
@@ -0,0 +1,5 @@
+---
+"@clerk/backend": patch
+---
+
+Fixed an issue when using multiple `acceptsToken` values in `authenticateRequest`. When `acceptsToken` is an array containing both session and machine token types (e.g., `['session_token', 'api_key']`), the function now correctly routes to the appropriate authentication handler based on the actual token type, instead of always treating them as machine tokens.
diff --git a/packages/backend/src/tokens/__tests__/request.test.ts b/packages/backend/src/tokens/__tests__/request.test.ts
index 0d140f8b093..450da616de5 100644
--- a/packages/backend/src/tokens/__tests__/request.test.ts
+++ b/packages/backend/src/tokens/__tests__/request.test.ts
@@ -1393,7 +1393,7 @@ describe('tokens.authenticateRequest(options)', () => {
     });
 
     describe('Array of Accepted Token Types', () => {
-      test('accepts token when it is in the acceptsToken array', async () => {
+      test('accepts machine token when it is in the acceptsToken array', async () => {
         server.use(
           http.post(mockMachineAuthResponses.api_key.endpoint, () => {
             return HttpResponse.json(mockVerificationResults.api_key);
@@ -1409,8 +1409,83 @@ describe('tokens.authenticateRequest(options)', () => {
         expect(requestState).toBeMachineAuthenticated();
       });
 
-      test('returns unauthenticated state when token type is not in the acceptsToken array', async () => {
+      test('accepts session token in header when session_token is in the acceptsToken array', async () => {
+        server.use(
+          http.get('https://api.clerk.test/v1/jwks', () => {
+            return HttpResponse.json(mockJwks);
+          }),
+        );
+
+        const request = mockRequest({ authorization: `Bearer ${mockJwt}` });
+        const requestState = await authenticateRequest(
+          request,
+          mockOptions({ acceptsToken: ['session_token', 'api_key'] }),
+        );
+
+        expect(requestState).toBeSignedIn();
+        expect(requestState.toAuth()).toBeSignedInToAuth();
+      });
+
+      test('accepts session token in cookie when session_token is in the acceptsToken array', async () => {
+        server.use(
+          http.get('https://api.clerk.test/v1/jwks', () => {
+            return HttpResponse.json(mockJwks);
+          }),
+        );
+
+        const requestState = await authenticateRequest(
+          mockRequestWithCookies(
+            {},
+            {
+              __session: mockJwt,
+              __client_uat: '12345',
+            },
+          ),
+          mockOptions({ acceptsToken: ['session_token', 'api_key'] }),
+        );
+
+        // The key assertion: session token is accepted (not rejected as invalid token)
+        // Cookie-based auth may trigger handshake flow, but should not return TokenTypeMismatch
+        expect(requestState.tokenType).not.toBeNull();
+        expect(requestState.reason).not.toBe(AuthErrorReason.TokenTypeMismatch);
+      });
+
+      test('accepts machine token when acceptsToken array contains mixed token types', async () => {
+        server.use(
+          http.post(mockMachineAuthResponses.m2m_token.endpoint, () => {
+            return HttpResponse.json(mockVerificationResults.m2m_token);
+          }),
+        );
+
         const request = mockRequest({ authorization: `Bearer ${mockTokens.m2m_token}` });
+        const requestState = await authenticateRequest(
+          request,
+          mockOptions({ acceptsToken: ['session_token', 'm2m_token'] }),
+        );
+
+        expect(requestState).toBeMachineAuthenticated();
+      });
+
+      test('returns unauthenticated state when machine token type is not in the acceptsToken array', async () => {
+        const request = mockRequest({ authorization: `Bearer ${mockTokens.m2m_token}` });
+        const requestState = await authenticateRequest(
+          request,
+          mockOptions({ acceptsToken: ['api_key', 'oauth_token'] }),
+        );
+
+        expect(requestState).toBeMachineUnauthenticated({
+          tokenType: null,
+          reason: AuthErrorReason.TokenTypeMismatch,
+          message: '',
+        });
+        expect(requestState.toAuth()).toBeMachineUnauthenticatedToAuth({
+          tokenType: null,
+          isAuthenticated: false,
+        });
+      });
+
+      test('returns unauthenticated state when session token is provided but not in the acceptsToken array', async () => {
+        const request = mockRequest({ authorization: `Bearer ${mockJwt}` });
         const requestState = await authenticateRequest(
           request,
           mockOptions({ acceptsToken: ['api_key', 'oauth_token'] }),
@@ -1426,6 +1501,25 @@ describe('tokens.authenticateRequest(options)', () => {
           isAuthenticated: false,
         });
       });
+
+      test('returns unauthenticated state when no token is provided and acceptsToken array contains only machine tokens', async () => {
+        const requestState = await authenticateRequest(
+          mockRequestWithCookies(
+            {},
+            {
+              __session: mockJwt,
+              __client_uat: '12345',
+            },
+          ),
+          mockOptions({ acceptsToken: ['api_key', 'm2m_token'] }),
+        );
+
+        expect(requestState).toBeMachineUnauthenticated({
+          tokenType: null,
+          reason: AuthErrorReason.TokenTypeMismatch,
+          message: '',
+        });
+      });
     });
 
     describe('Token Location Validation', () => {
diff --git a/packages/backend/src/tokens/request.ts b/packages/backend/src/tokens/request.ts
index 863afeabaa4..88999fedc0c 100644
--- a/packages/backend/src/tokens/request.ts
+++ b/packages/backend/src/tokens/request.ts
@@ -782,7 +782,7 @@ export const authenticateRequest: AuthenticateRequest = (async (
   }
 
   if (authenticateContext.tokenInHeader) {
-    if (acceptsToken === 'any') {
+    if (acceptsToken === 'any' || Array.isArray(acceptsToken)) {
       return authenticateAnyRequestWithTokenInHeader();
     }
     if (acceptsToken === TokenType.SessionToken) {