diff --git a/packages/http/src/HttpRequestFailed.php b/packages/http/src/HttpRequestFailed.php
index b207921de..c5fd3aade 100644
--- a/packages/http/src/HttpRequestFailed.php
+++ b/packages/http/src/HttpRequestFailed.php
@@ -15,12 +15,14 @@ final class HttpRequestFailed extends Exception implements ProvidesContext
      * @param string|null $message An optional message that will be displayed to the client.
      * @param Response|null $cause The response that caused the failure, if any.
      * @param Request|null $request The request that failed, for debug purposes.
+     * @param array<string, string|string[]> $headers Headers that the response must carry, such as `retry-after` on a `429`.
      */
     public function __construct(
         private(set) readonly Status $status,
         ?string $message = null,
         private(set) readonly ?Response $cause = null,
         private(set) readonly ?Request $request = null,
+        private(set) readonly array $headers = [],
     ) {
         parent::__construct(
             message: $message ?: '',
diff --git a/packages/router/src/Exceptions/HttpExceptionHandler.php b/packages/router/src/Exceptions/HttpExceptionHandler.php
index da5562651..3d366178b 100644
--- a/packages/router/src/Exceptions/HttpExceptionHandler.php
+++ b/packages/router/src/Exceptions/HttpExceptionHandler.php
@@ -7,6 +7,7 @@
 use Tempest\Core\Exceptions\ExceptionProcessor;
 use Tempest\Core\Kernel;
 use Tempest\Http\GenericResponse;
+use Tempest\Http\HttpRequestFailed;
 use Tempest\Http\Request;
 use Tempest\Http\Response;
 use Tempest\Http\Status;
@@ -46,10 +47,33 @@ public function renderResponse(Request $request, Throwable $throwable): Response
             $renderer = $this->container->get($rendererClass);
 
             if ($renderer->canRender($throwable, $request)) {
-                return $renderer->render($throwable);
+                return $this->applyHeaders($renderer->render($throwable), $throwable);
             }
         }
 
         return new GenericResponse(status: Status::NOT_ACCEPTABLE);
     }
+
+    /**
+     * Applies the headers declared by a failure, which renderers would otherwise discard by building a response from scratch.
+     */
+    private function applyHeaders(Response $response, Throwable $throwable): Response
+    {
+        if (! $throwable instanceof HttpRequestFailed) {
+            return $response;
+        }
+
+        foreach ($throwable->headers as $name => $values) {
+            // Headers keep the casing they were added with, so we look up the existing one to avoid a duplicate
+            $existing = $response->getHeader($name);
+
+            $response->removeHeader($existing === null ? $name : $existing->name);
+
+            foreach (is_array($values) ? $values : [$values] as $value) {
+                $response->addHeader($name, $value);
+            }
+        }
+
+        return $response;
+    }
 }
diff --git a/tests/Integration/Http/Exceptions/HttpExceptionHandlerTest.php b/tests/Integration/Http/Exceptions/HttpExceptionHandlerTest.php
index a20f427ea..430f15d29 100644
--- a/tests/Integration/Http/Exceptions/HttpExceptionHandlerTest.php
+++ b/tests/Integration/Http/Exceptions/HttpExceptionHandlerTest.php
@@ -12,6 +12,7 @@
 use Tempest\Core\Kernel;
 use Tempest\Http\HttpRequestFailed;
 use Tempest\Http\Response;
+use Tempest\Http\Responses\Json;
 use Tempest\Http\Responses\Redirect;
 use Tempest\Http\Status;
 use Tempest\Router\Exceptions\HttpExceptionHandler;
@@ -132,6 +133,53 @@ public function exception_handler_returns_same_code_as_http_exception(Status $st
         $this->assertSame($status, $this->response->status);
     }
 
+    #[Test]
+    public function exception_handler_applies_headers_declared_on_the_exception(): void
+    {
+        $this->callExceptionHandler(function (): void {
+            $handler = $this->container->get(HttpExceptionHandler::class);
+            $handler->handle(new HttpRequestFailed(
+                status: Status::UNAUTHORIZED,
+                headers: ['www-authenticate' => 'Bearer'],
+            ));
+        });
+
+        $this->assertContains('Bearer', $this->response->getHeader('www-authenticate')->values);
+    }
+
+    #[Test]
+    public function exception_handler_replaces_headers_that_the_rendered_response_already_carries(): void
+    {
+        // The renderer forwards a cause that has a body, so the response it returns already carries the header
+        $cause = new Json(body: ['message' => 'Slow down.'], status: Status::TOO_MANY_REQUESTS)
+            ->addHeader('Retry-After', '30');
+
+        $this->callExceptionHandler(function () use ($cause): void {
+            $handler = $this->container->get(HttpExceptionHandler::class);
+            $handler->handle(new HttpRequestFailed(
+                status: Status::TOO_MANY_REQUESTS,
+                cause: $cause,
+                headers: ['retry-after' => '60'],
+            ));
+        });
+
+        $this->assertSame(['60'], $this->response->getHeader('retry-after')->values);
+    }
+
+    #[Test]
+    public function exception_handler_applies_every_value_of_a_declared_header(): void
+    {
+        $this->callExceptionHandler(function (): void {
+            $handler = $this->container->get(HttpExceptionHandler::class);
+            $handler->handle(new HttpRequestFailed(
+                status: Status::METHOD_NOT_ALLOWED,
+                headers: ['allow' => ['GET', 'HEAD']],
+            ));
+        });
+
+        $this->assertSame(['GET', 'HEAD'], $this->response->getHeader('allow')->values);
+    }
+
     #[Test]
     public function exception_handler_runs_exception_processors(): void
     {