diff --git a/lib/error-handler.js b/lib/error-handler.js
index 0b9dbdbb99..cde82f8bae 100644
--- a/lib/error-handler.js
+++ b/lib/error-handler.js
@@ -65,13 +65,17 @@ function handleError (reply, error, cb) {
     return
   }
 
-  const result = func(error, reply.request, reply)
-  if (result !== undefined) {
-    if (result !== null && typeof result.then === 'function') {
-      wrapThenable(result, reply)
-    } else {
-      reply.send(result)
+  try {
+    const result = func(error, reply.request, reply)
+    if (result !== undefined) {
+      if (result !== null && typeof result.then === 'function') {
+        wrapThenable(result, reply)
+      } else {
+        reply.send(result)
+      }
     }
+  } catch (err) {
+    reply.send(err)
   }
 }
 
diff --git a/lib/wrapThenable.js b/lib/wrapThenable.js
index b746a62e92..abb75bdd03 100644
--- a/lib/wrapThenable.js
+++ b/lib/wrapThenable.js
@@ -39,6 +39,8 @@ function wrapThenable (thenable, reply) {
     // try-catch allow to re-throw error in error handler for async handler
     try {
       reply.send(err)
+      // The following should not happen
+      /* c8 ignore next 3 */
     } catch (err) {
       reply.send(err)
     }
diff --git a/test/500s.test.js b/test/500s.test.js
index 3422fcfec4..3c915dba0a 100644
--- a/test/500s.test.js
+++ b/test/500s.test.js
@@ -188,3 +188,35 @@ test('cannot set childLoggerFactory after binding', t => {
     }
   })
 })
+
+test('catch synchronous errors', t => {
+  t.plan(3)
+
+  const fastify = Fastify()
+  t.teardown(fastify.close.bind(fastify))
+
+  fastify.setErrorHandler((_, req, reply) => {
+    throw new Error('kaboom2')
+  })
+
+  fastify.post('/', function (req, reply) {
+    reply.send(new Error('kaboom'))
+  })
+
+  fastify.inject({
+    method: 'POST',
+    url: '/',
+    headers: {
+      'Content-Type': 'application/json'
+    },
+    payload: JSON.stringify({ hello: 'world' }).substring(0, 5)
+  }, (err, res) => {
+    t.error(err)
+    t.equal(res.statusCode, 500)
+    t.same(res.json(), {
+      error: 'Internal Server Error',
+      message: 'kaboom2',
+      statusCode: 500
+    })
+  })
+})
diff --git a/test/types/request.test-d.ts b/test/types/request.test-d.ts
index fd3359bab3..dfd4b78702 100644
--- a/test/types/request.test-d.ts
+++ b/test/types/request.test-d.ts
@@ -81,8 +81,8 @@ const getHandler: RouteHandler = function (request, _reply) {
   expectType<FastifyRequestContext<ContextConfigDefault>['config']>(request.routeConfig)
   expectType<FastifyRequestContext<ContextConfigDefault>['config']>(request.routeOptions.config)
   expectType<ContextConfigDefault & FastifyRouteConfig & FastifyContextConfig>(request.routeOptions.config)
-  expectType<FastifySchema>(request.routeSchema)
-  expectType<FastifySchema>(request.routeOptions.schema)
+  expectType<FastifySchema | undefined>(request.routeSchema)
+  expectType<FastifySchema | undefined>(request.routeOptions.schema)
   expectType<RouteHandlerMethod>(request.routeOptions.handler)
   expectType<string | undefined>(request.routeOptions.url)
 
diff --git a/types/request.d.ts b/types/request.d.ts
index b1b82c6e61..b2e4e38ec5 100644
--- a/types/request.d.ts
+++ b/types/request.d.ts
@@ -31,7 +31,7 @@ export interface RequestRouteOptions<ContextConfig = ContextConfigDefault, Schem
   exposeHeadRoute: boolean;
   prefixTrailingSlash: string;
   config: FastifyContextConfig & FastifyRouteConfig & ContextConfig;
-  schema: SchemaCompiler;
+  schema?: SchemaCompiler; // it is empty for 404 requests
   handler: RouteHandlerMethod;
 }
 
@@ -64,7 +64,7 @@ export interface FastifyRequest<RouteGeneric extends RouteGenericInterface = Rou
   body: RequestType['body'];
   context: FastifyRequestContext<ContextConfig>;
   routeConfig: FastifyRequestContext<ContextConfig>['config'];
-  routeSchema: FastifySchema
+  routeSchema?: FastifySchema; // it is empty for 404 requests
 
   /** in order for this to be used the user should ensure they have set the attachValidation option. */
   validationError?: Error & { validation: any; validationContext: string };