diff --git a/packages/http/src/Session/VerifyCsrfMiddleware.php b/packages/http/src/Session/VerifyCsrfMiddleware.php
index 0e00063f2..be9aa1a3a 100644
--- a/packages/http/src/Session/VerifyCsrfMiddleware.php
+++ b/packages/http/src/Session/VerifyCsrfMiddleware.php
@@ -7,6 +7,8 @@
 use Tempest\Clock\Clock;
 use Tempest\Core\AppConfig;
 use Tempest\Core\Priority;
+use Tempest\Cryptography\Encryption\Encrypter;
+use Tempest\Cryptography\Encryption\Exceptions\EncryptionException;
 use Tempest\Http\Cookie\Cookie;
 use Tempest\Http\Cookie\CookieManager;
 use Tempest\Http\Method;
@@ -15,6 +17,7 @@
 use Tempest\Http\Session\Session;
 use Tempest\Router\HttpMiddleware;
 use Tempest\Router\HttpMiddlewareCallable;
+use Tempest\Support\Json\Exception\JsonCouldNotBeDecoded;
 use Tempest\Support\Str;
 
 #[Priority(Priority::FRAMEWORK)]
@@ -29,6 +32,7 @@ public function __construct(
         private SessionConfig $sessionConfig,
         private CookieManager $cookies,
         private Clock $clock,
+        private Encrypter $encrypter,
     ) {}
 
     public function __invoke(Request $request, HttpMiddlewareCallable $next): Response
@@ -67,9 +71,18 @@ private function ensureTokenMatches(Request $request): void
     {
         $tokenFromRequest = $request->get(
             key: Session::CSRF_TOKEN_KEY,
-            default: $request->headers->get(self::CSRF_HEADER_KEY),
         );
 
+        if (! $tokenFromRequest && $request->headers->has(self::CSRF_HEADER_KEY)) {
+            try {
+                $tokenFromRequest = $this->encrypter->decrypt(
+                    urldecode($request->headers->get(self::CSRF_HEADER_KEY)),
+                );
+            } catch (EncryptionException|JsonCouldNotBeDecoded) {
+                throw new CsrfTokenDidNotMatch();
+            }
+        }
+
         if (! $tokenFromRequest) {
             throw new CsrfTokenDidNotMatch();
         }
diff --git a/tests/Integration/Http/CsrfTest.php b/tests/Integration/Http/CsrfTest.php
index 0980840cd..3c6d2ff92 100644
--- a/tests/Integration/Http/CsrfTest.php
+++ b/tests/Integration/Http/CsrfTest.php
@@ -5,6 +5,7 @@
 use PHPUnit\Framework\Attributes\TestWith;
 use Tempest\Core\AppConfig;
 use Tempest\Core\Environment;
+use Tempest\Cryptography\Encryption\Encrypter;
 use Tempest\Http\Cookie\Cookie;
 use Tempest\Http\GenericRequest;
 use Tempest\Http\Method;
@@ -84,17 +85,35 @@ public function test_matches_from_body(): void
             ->assertOk();
     }
 
-    public function test_matches_from_header(): void
+    public function test_matches_from_header_when_encrypted(): void
     {
         $this->container->get(AppConfig::class)->environment = Environment::PRODUCTION;
-
         $session = $this->container->get(Session::class);
 
+        // Encrypt the token as it would be in a real request
+        $sessionCookieValue = $this->container
+            ->get(Encrypter::class)
+            ->encrypt($session->token)
+            ->serialize();
+
         $this->http
-            ->post('/test', headers: [VerifyCsrfMiddleware::CSRF_HEADER_KEY => $session->token])
+            ->post('/test', headers: [VerifyCsrfMiddleware::CSRF_HEADER_KEY => $sessionCookieValue])
             ->assertOk();
     }
 
+    public function test_throws_csrf_exception_when_header_is_non_serialized_hash(): void
+    {
+        $this->expectException(CsrfTokenDidNotMatch::class);
+        $this->container->get(AppConfig::class)->environment = Environment::PRODUCTION;
+        $session = $this->container->get(Session::class);
+
+        // simulate a non-serialized hash
+        $sessionCookieValue = 'i-am-not-correct';
+
+        $this->http
+            ->post('/test', headers: [VerifyCsrfMiddleware::CSRF_HEADER_KEY => $sessionCookieValue]);
+    }
+
     public function test_csrf_component(): void
     {
         $session = $this->container->get(Session::class);