diff --git a/packages/core/src/DevelopmentExceptionHandler.php b/packages/core/src/DevelopmentExceptionHandler.php
deleted file mode 100644
index cf4d28db2..000000000
--- a/packages/core/src/DevelopmentExceptionHandler.php
+++ /dev/null
@@ -1,64 +0,0 @@
-<?php
-
-namespace Tempest\Core;
-
-use Tempest\Container\Container;
-use Tempest\Http\Request;
-use Tempest\Router\MatchedRoute;
-use Throwable;
-use Whoops\Handler\HandlerInterface;
-use Whoops\Handler\PrettyPageHandler;
-use Whoops\Run;
-
-final readonly class DevelopmentExceptionHandler implements ExceptionHandler
-{
-    private Run $whoops;
-
-    public function __construct(
-        private Container $container,
-        private ExceptionReporter $exceptionReporter,
-    ) {
-        $this->whoops = new Run();
-        $this->whoops->pushHandler($this->createHandler());
-    }
-
-    public function handle(Throwable $throwable): void
-    {
-        $this->exceptionReporter->report($throwable);
-        $this->whoops->handleException($throwable);
-    }
-
-    private function createHandler(): HandlerInterface
-    {
-        $handler = new PrettyPageHandler();
-
-        $handler->addDataTableCallback('Route', function () {
-            $route = $this->container->get(MatchedRoute::class);
-
-            if (! $route) {
-                return [];
-            }
-
-            return [
-                'Handler' => $route->route->handler->getDeclaringClass()->getFileName() . ':' . $route->route->handler->getName(),
-                'URI' => $route->route->uri,
-                'Allowed parameters' => $route->route->parameters,
-                'Received parameters' => $route->params,
-            ];
-        });
-
-        $handler->addDataTableCallback('Request', function () {
-            $request = $this->container->get(Request::class);
-
-            return [
-                'URI' => $request->uri,
-                'Method' => $request->method->value,
-                'Headers' => $request->headers->toArray(),
-                'Parsed body' => array_filter(array_values($request->body)) ? $request->body : [],
-                'Raw body' => $request->raw,
-            ];
-        });
-
-        return $handler;
-    }
-}
diff --git a/packages/core/src/ExceptionHandlerInitializer.php b/packages/core/src/ExceptionHandlerInitializer.php
index fe3e24e01..a4a291cd1 100644
--- a/packages/core/src/ExceptionHandlerInitializer.php
+++ b/packages/core/src/ExceptionHandlerInitializer.php
@@ -17,7 +17,6 @@ public function initialize(Container $container): ExceptionHandler
 
         return match (true) {
             PHP_SAPI === 'cli' => $container->get(ConsoleExceptionHandler::class),
-            $config->environment->isLocal() => $container->get(DevelopmentExceptionHandler::class),
             default => $container->get(HttpExceptionHandler::class),
         };
     }
diff --git a/packages/http/src/Responses/NotAcceptable.php b/packages/http/src/Responses/NotAcceptable.php
new file mode 100644
index 000000000..5336039a0
--- /dev/null
+++ b/packages/http/src/Responses/NotAcceptable.php
@@ -0,0 +1,19 @@
+<?php
+
+declare(strict_types=1);
+
+namespace Tempest\Http\Responses;
+
+use Tempest\Http\IsResponse;
+use Tempest\Http\Response;
+use Tempest\Http\Status;
+
+final class NotAcceptable implements Response
+{
+    use IsResponse;
+
+    public function __construct()
+    {
+        $this->status = Status::NOT_ACCEPTABLE;
+    }
+}
diff --git a/packages/router/src/Exceptions/HtmlExceptionRenderer.php b/packages/router/src/Exceptions/HtmlExceptionRenderer.php
new file mode 100644
index 000000000..606789c30
--- /dev/null
+++ b/packages/router/src/Exceptions/HtmlExceptionRenderer.php
@@ -0,0 +1,119 @@
+<?php
+
+namespace Tempest\Router\Exceptions;
+
+use Tempest\Auth\Exceptions\AccessWasDenied;
+use Tempest\Container\Container;
+use Tempest\Core\AppConfig;
+use Tempest\Http\GenericResponse;
+use Tempest\Http\HttpRequestFailed;
+use Tempest\Http\Request;
+use Tempest\Http\Response;
+use Tempest\Http\Responses\Invalid;
+use Tempest\Http\Session\CsrfTokenDidNotMatch;
+use Tempest\Http\Status;
+use Tempest\Router\MatchedRoute;
+use Tempest\Support\Filesystem;
+use Tempest\Validation\Exceptions\ValidationFailed;
+use Tempest\View\GenericView;
+use Throwable;
+use Whoops\Handler\PrettyPageHandler;
+use Whoops\Run;
+
+final readonly class HtmlExceptionRenderer
+{
+    public function __construct(
+        private AppConfig $appConfig,
+        private Container $container,
+    ) {}
+
+    public function render(Throwable $throwable): Response
+    {
+        if ($throwable instanceof ConvertsToResponse) {
+            return $throwable->toResponse();
+        }
+
+        if ($this->appConfig->environment->isLocal()) {
+            $whoops = $this->createHandler();
+
+            return new GenericResponse(
+                status: Status::INTERNAL_SERVER_ERROR,
+                body: $whoops->handleException($throwable),
+            );
+        }
+
+        return match (true) {
+            $throwable instanceof RouteBindingFailed => $this->renderErrorResponse(Status::NOT_FOUND),
+            $throwable instanceof ValidationFailed => new Invalid($throwable->subject, $throwable->failingRules),
+            $throwable instanceof AccessWasDenied => $this->renderErrorResponse(Status::FORBIDDEN),
+            $throwable instanceof HttpRequestFailed => $this->renderErrorResponse($throwable->status, $throwable),
+            $throwable instanceof CsrfTokenDidNotMatch => $this->renderErrorResponse(Status::UNPROCESSABLE_CONTENT),
+            default => $this->renderErrorResponse(Status::INTERNAL_SERVER_ERROR),
+        };
+    }
+
+    private function renderErrorResponse(Status $status, ?Throwable $exception = null): Response
+    {
+        return new GenericResponse(
+            status: $status,
+            body: new GenericView(__DIR__ . '/HttpErrorResponse/error.view.php', [
+                'css' => $this->getStyleSheet(),
+                'status' => $status->value,
+                'title' => $status->description(),
+                'message' => $exception?->getMessage() ?: match ($status) {
+                    Status::INTERNAL_SERVER_ERROR => 'An unexpected server error occurred',
+                    Status::NOT_FOUND => 'This page could not be found on the server',
+                    Status::FORBIDDEN => 'You do not have permission to access this page',
+                    Status::UNAUTHORIZED => 'You must be authenticated in to access this page',
+                    Status::UNPROCESSABLE_CONTENT => 'The request could not be processed due to invalid data',
+                    default => null,
+                },
+            ]),
+        );
+    }
+
+    private function getStyleSheet(): string
+    {
+        return Filesystem\read_file(__DIR__ . '/HttpErrorResponse/style.css');
+    }
+
+    private function createHandler(): Run
+    {
+        $handler = new PrettyPageHandler();
+
+        $handler->addDataTableCallback('Route', function () {
+            $route = $this->container->get(MatchedRoute::class);
+
+            if (! $route) {
+                return [];
+            }
+
+            return [
+                'Handler' => $route->route->handler->getDeclaringClass()->getFileName() . ':' . $route->route->handler->getName(),
+                'URI' => $route->route->uri,
+                'Allowed parameters' => $route->route->parameters,
+                'Received parameters' => $route->params,
+            ];
+        });
+
+        $handler->addDataTableCallback('Request', function () {
+            $request = $this->container->get(Request::class);
+
+            return [
+                'URI' => $request->uri,
+                'Method' => $request->method->value,
+                'Headers' => $request->headers->toArray(),
+                'Parsed body' => array_filter(array_values($request->body)) ? $request->body : [],
+                'Raw body' => $request->raw,
+            ];
+        });
+
+        $whoops = new Run();
+
+        $whoops->pushHandler($handler);
+
+        $whoops->writeToOutput(send: false);
+
+        return $whoops;
+    }
+}
diff --git a/packages/router/src/Exceptions/HttpExceptionHandler.php b/packages/router/src/Exceptions/HttpExceptionHandler.php
index fe093c0b0..9bcb6bc75 100644
--- a/packages/router/src/Exceptions/HttpExceptionHandler.php
+++ b/packages/router/src/Exceptions/HttpExceptionHandler.php
@@ -2,20 +2,16 @@
 
 namespace Tempest\Router\Exceptions;
 
-use Tempest\Auth\Exceptions\AccessWasDenied;
 use Tempest\Container\Container;
 use Tempest\Core\AppConfig;
 use Tempest\Core\ExceptionHandler;
 use Tempest\Core\ExceptionReporter;
 use Tempest\Core\Kernel;
+use Tempest\Http\ContentType;
 use Tempest\Http\GenericResponse;
-use Tempest\Http\HttpRequestFailed;
-use Tempest\Http\Response;
-use Tempest\Http\Session\CsrfTokenDidNotMatch;
+use Tempest\Http\Request;
 use Tempest\Http\Status;
 use Tempest\Router\ResponseSender;
-use Tempest\Support\Filesystem;
-use Tempest\View\GenericView;
 use Throwable;
 
 final readonly class HttpExceptionHandler implements ExceptionHandler
@@ -26,19 +22,21 @@ public function __construct(
         private ResponseSender $responseSender,
         private Container $container,
         private ExceptionReporter $exceptionReporter,
+        private JsonExceptionRenderer $jsonHandler,
+        private HtmlExceptionRenderer $htmlHandler,
     ) {}
 
     public function handle(Throwable $throwable): void
     {
+        $request = $this->container->get(Request::class);
+
         try {
             $this->exceptionReporter->report($throwable);
 
             $response = match (true) {
-                $throwable instanceof ConvertsToResponse => $throwable->toResponse(),
-                $throwable instanceof AccessWasDenied => $this->renderErrorResponse(Status::FORBIDDEN),
-                $throwable instanceof HttpRequestFailed => $this->renderErrorResponse($throwable->status, $throwable),
-                $throwable instanceof CsrfTokenDidNotMatch => $this->renderErrorResponse(Status::UNPROCESSABLE_CONTENT),
-                default => $this->renderErrorResponse(Status::INTERNAL_SERVER_ERROR),
+                $request->accepts(ContentType::HTML, ContentType::XHTML) => $this->htmlHandler->render($throwable),
+                $request->accepts(ContentType::JSON) => $this->jsonHandler->render($throwable),
+                default => new GenericResponse(status: Status::NOT_ACCEPTABLE),
             };
 
             $this->responseSender->send($response);
@@ -46,29 +44,4 @@ public function handle(Throwable $throwable): void
             $this->kernel->shutdown();
         }
     }
-
-    private function renderErrorResponse(Status $status, ?HttpRequestFailed $exception = null): Response
-    {
-        return new GenericResponse(
-            status: $status,
-            body: new GenericView(__DIR__ . '/HttpErrorResponse/error.view.php', [
-                'css' => $this->getStyleSheet(),
-                'status' => $status->value,
-                'title' => $status->description(),
-                'message' => $exception?->getMessage() ?: match ($status) {
-                    Status::INTERNAL_SERVER_ERROR => 'An unexpected server error occurred',
-                    Status::NOT_FOUND => 'This page could not be found on the server',
-                    Status::FORBIDDEN => 'You do not have permission to access this page',
-                    Status::UNAUTHORIZED => 'You must be authenticated in to access this page',
-                    Status::UNPROCESSABLE_CONTENT => 'The request could not be processed due to invalid data',
-                    default => null,
-                },
-            ]),
-        );
-    }
-
-    private function getStyleSheet(): string
-    {
-        return Filesystem\read_file(__DIR__ . '/HttpErrorResponse/style.css');
-    }
 }
diff --git a/packages/router/src/Exceptions/JsonExceptionRenderer.php b/packages/router/src/Exceptions/JsonExceptionRenderer.php
new file mode 100644
index 000000000..f60b12e58
--- /dev/null
+++ b/packages/router/src/Exceptions/JsonExceptionRenderer.php
@@ -0,0 +1,84 @@
+<?php
+
+namespace Tempest\Router\Exceptions;
+
+use Tempest\Auth\Exceptions\AccessWasDenied;
+use Tempest\Core\AppConfig;
+use Tempest\Http\HttpRequestFailed;
+use Tempest\Http\Response;
+use Tempest\Http\Responses\Json;
+use Tempest\Http\Session\CsrfTokenDidNotMatch;
+use Tempest\Http\Status;
+use Tempest\Validation\Exceptions\ValidationFailed;
+use Tempest\Validation\Rule;
+use Tempest\Validation\Validator;
+use Throwable;
+
+use function Tempest\Support\arr;
+
+final readonly class JsonExceptionRenderer
+{
+    public function __construct(
+        private AppConfig $appConfig,
+        private Validator $validator,
+    ) {}
+
+    public function render(Throwable $throwable): Response
+    {
+        return match (true) {
+            $throwable instanceof ConvertsToResponse => $throwable->toResponse(),
+            $throwable instanceof ValidationFailed => $this->renderValidationErrorResponse($throwable),
+            $throwable instanceof RouteBindingFailed => $this->renderErrorResponse(Status::NOT_FOUND),
+            $throwable instanceof AccessWasDenied => $this->renderErrorResponse(Status::FORBIDDEN),
+            $throwable instanceof HttpRequestFailed => $this->renderErrorResponse($throwable->status, $throwable),
+            $throwable instanceof CsrfTokenDidNotMatch => $this->renderErrorResponse(Status::UNPROCESSABLE_CONTENT),
+            default => $this->renderErrorResponse(Status::INTERNAL_SERVER_ERROR, $throwable),
+        };
+    }
+
+    private function renderValidationErrorResponse(ValidationFailed $exception): Response
+    {
+        $errors = arr($exception->failingRules)->map(
+            fn (array $failingRulesForField, string $field) => arr($failingRulesForField)->map(
+                fn (Rule $rule) => $this->validator->getErrorMessage($rule, $field),
+            )->toArray(),
+        );
+
+        return new Json([
+            'message' => $errors->first()[0],
+            'errors' => $errors->toArray(),
+        ])->setStatus(Status::UNPROCESSABLE_CONTENT);
+    }
+
+    private function renderErrorResponse(Status $status, ?Throwable $exception = null): Response
+    {
+        return new Json(
+            $this->appConfig->environment->isLocal() && $exception !== null
+                ? [
+                    'message' => static::getErrorMessage($status, $exception),
+                    'exception' => get_class($exception),
+                    'file' => $exception->getFile(),
+                    'line' => $exception->getLine(),
+                    'trace' => arr($exception->getTrace())->map(
+                        fn ($trace) => arr($trace)->removeKeys('args')->toArray(),
+                    )->toArray(),
+                ] : [
+                    'message' => static::getErrorMessage($status, $exception),
+                ],
+        )->setStatus($status);
+    }
+
+    private static function getErrorMessage(Status $status, ?Throwable $exception = null): ?string
+    {
+        return (
+            $exception?->getMessage() ?: match ($status) {
+                Status::INTERNAL_SERVER_ERROR => 'An unexpected server error occurred',
+                Status::NOT_FOUND => 'This page could not be found on the server',
+                Status::FORBIDDEN => 'You do not have permission to access this page',
+                Status::UNAUTHORIZED => 'You must be authenticated in to access this page',
+                Status::UNPROCESSABLE_CONTENT => 'The request could not be processed due to invalid data',
+                default => $status->description(),
+            }
+        );
+    }
+}
diff --git a/packages/router/src/HandleRouteExceptionMiddleware.php b/packages/router/src/HandleRouteExceptionMiddleware.php
index 72188081c..81bbf2b9a 100644
--- a/packages/router/src/HandleRouteExceptionMiddleware.php
+++ b/packages/router/src/HandleRouteExceptionMiddleware.php
@@ -3,12 +3,15 @@
 namespace Tempest\Router;
 
 use Tempest\Core\Priority;
+use Tempest\Http\ContentType;
 use Tempest\Http\HttpRequestFailed;
 use Tempest\Http\Request;
 use Tempest\Http\Response;
 use Tempest\Http\Responses\Invalid;
+use Tempest\Http\Responses\NotAcceptable;
 use Tempest\Http\Responses\NotFound;
 use Tempest\Router\Exceptions\ConvertsToResponse;
+use Tempest\Router\Exceptions\JsonExceptionRenderer;
 use Tempest\Router\Exceptions\RouteBindingFailed;
 use Tempest\Validation\Exceptions\ValidationFailed;
 
@@ -17,6 +20,7 @@
 {
     public function __construct(
         private RouteConfig $routeConfig,
+        private JsonExceptionRenderer $jsonHandler,
     ) {}
 
     public function __invoke(Request $request, HttpMiddlewareCallable $next): Response
@@ -44,9 +48,19 @@ private function forward(Request $request, HttpMiddlewareCallable $next): Respon
             return $next($request);
         } catch (ConvertsToResponse $convertsToResponse) {
             return $convertsToResponse->toResponse();
-        } catch (RouteBindingFailed) {
-            return new NotFound();
+        } catch (RouteBindingFailed $routeBindingFailed) {
+            return match (true) {
+                $request->accepts(ContentType::HTML, ContentType::XHTML) => new NotFound(),
+                $request->accepts(ContentType::JSON) => $this->jsonHandler->render($routeBindingFailed),
+                default => new NotAcceptable(),
+            };
         } catch (ValidationFailed $validationException) {
+            return match (true) {
+                $request->accepts(ContentType::HTML, ContentType::XHTML) => new Invalid($validationException->subject, $validationException->failingRules),
+                $request->accepts(ContentType::JSON) => $this->jsonHandler->render($validationException),
+                default => new NotAcceptable(),
+            };
+
             return new Invalid($validationException->subject, $validationException->failingRules);
         }
     }
diff --git a/tests/Integration/Route/RouterTest.php b/tests/Integration/Route/RouterTest.php
index 3b1af2dcd..a4f12c1b3 100644
--- a/tests/Integration/Route/RouterTest.php
+++ b/tests/Integration/Route/RouterTest.php
@@ -245,6 +245,16 @@ public function test_converts_to_response(): void
             ->assertHeaderContains('Location', 'https://tempestphp.com');
     }
 
+    public function test_router_returns_json_exception_when_accepts_json(): void
+    {
+        $this->registerRoute([Http500Controller::class, 'throwsException']);
+
+        $this->http
+            ->get('/throws-exception', headers: ['Accept' => 'application/json'])
+            ->assertStatus(Status::INTERNAL_SERVER_ERROR)
+            ->assertJsonHasKeys('message');
+    }
+
     public function test_head_requests(): void
     {
         $this->registerRoute([HeadController::class, 'implicitHead']);