diff --git a/src/core/config/resolvers/error.ts b/src/core/config/resolvers/error.ts
index 3ea54ff672..346903b139 100644
--- a/src/core/config/resolvers/error.ts
+++ b/src/core/config/resolvers/error.ts
@@ -4,9 +4,13 @@ import { join } from "pathe";
 
 export async function resolveErrorOptions(options: NitroOptions) {
   if (!options.errorHandler) {
-    options.errorHandler = join(
-      runtimeDir,
-      `internal/error/${options.dev ? "dev" : "prod"}`
-    );
+    options.errorHandler = [];
+  } else if (!Array.isArray(options.errorHandler)) {
+    options.errorHandler = [options.errorHandler];
   }
+
+  // Always add the default error handler as the last one
+  options.errorHandler.push(
+    join(runtimeDir, `internal/error/${options.dev ? "dev" : "prod"}`)
+  );
 }
diff --git a/src/rollup/config.ts b/src/rollup/config.ts
index 853fdd2202..c51dc28bf0 100644
--- a/src/rollup/config.ts
+++ b/src/rollup/config.ts
@@ -41,6 +41,7 @@ import { sourcemapMininify } from "./plugins/sourcemap-min";
 import { storage } from "./plugins/storage";
 import { timing } from "./plugins/timing";
 import { virtual } from "./plugins/virtual";
+import { errorHandler } from "./plugins/error-handler";
 import { resolveAliases } from "./utils";
 
 export const getRollupConfig = (nitro: Nitro): RollupConfig => {
@@ -344,6 +345,9 @@ export const getRollupConfig = (nitro: Nitro): RollupConfig => {
     rollupConfig.plugins.push(handlersMeta(nitro));
   }
 
+  // Error handler
+  rollupConfig.plugins.push(errorHandler(nitro));
+
   // Polyfill
   rollupConfig.plugins.push(
     virtual(
@@ -393,7 +397,6 @@ export const plugins = [
     alias({
       entries: resolveAliases({
         "#build": buildDir,
-        "#nitro-internal-virtual/error-handler": nitro.options.errorHandler,
         "#internal/nitro": runtimeDir,
         "nitro/runtime": runtimeDir,
         "nitropack/runtime": runtimeDir,
diff --git a/src/rollup/plugins/error-handler.ts b/src/rollup/plugins/error-handler.ts
new file mode 100644
index 0000000000..15a74e6fe3
--- /dev/null
+++ b/src/rollup/plugins/error-handler.ts
@@ -0,0 +1,36 @@
+import type { Nitro } from "nitropack/types";
+import { virtual } from "./virtual";
+
+export function errorHandler(nitro: Nitro) {
+  return virtual(
+    {
+      "#nitro-internal-virtual/error-handler": () => {
+        const errorHandlers = Array.isArray(nitro.options.errorHandler)
+          ? nitro.options.errorHandler
+          : [nitro.options.errorHandler];
+
+        return /* js */ `
+${errorHandlers.map((h, i) => `import errorHandler$${i} from "${h}";`).join("\n")}
+
+const errorHandlers = [${errorHandlers.map((_, i) => `errorHandler$${i}`).join(", ")}];
+
+export default async function(error, event) {
+  for (const handler of errorHandlers) {
+    try {
+      await handler(error, event);
+      if (event.handled) {
+        return; // Response handled
+      }
+    } catch(error) {
+      // Handler itself thrown, log and continue
+      console.error(error);
+    }
+  }
+  // H3 will handle fallback
+}
+`;
+      },
+    },
+    nitro.vfs
+  );
+}
diff --git a/src/types/config.ts b/src/types/config.ts
index 2f05620180..d0d85b2239 100644
--- a/src/types/config.ts
+++ b/src/types/config.ts
@@ -181,7 +181,7 @@ export interface NitroOptions extends PresetOptions {
   handlers: NitroEventHandler[];
   routeRules: { [path: string]: NitroRouteRules };
   devHandlers: NitroDevEventHandler[];
-  errorHandler: string;
+  errorHandler: string | string[];
   devErrorHandler: NitroErrorHandler;
   prerender: {
     /**
diff --git a/test/fixture/error.ts b/test/fixture/error.ts
new file mode 100644
index 0000000000..b57d486090
--- /dev/null
+++ b/test/fixture/error.ts
@@ -0,0 +1,5 @@
+export default defineNitroErrorHandler((error, event) => {
+  if (event.path.includes("?custom_error_handler")) {
+    return send(event, "custom_error_handler");
+  }
+});
diff --git a/test/fixture/nitro.config.ts b/test/fixture/nitro.config.ts
index 94c64f63fb..c97856c2f1 100644
--- a/test/fixture/nitro.config.ts
+++ b/test/fixture/nitro.config.ts
@@ -81,6 +81,7 @@ export default defineNitroConfig({
     "db:migrate": { description: "Migrate database" },
     "db:seed": { description: "Seed database" },
   },
+  errorHandler: "~/error.ts",
   routeRules: {
     "/api/param/prerender4": { prerender: true },
     "/api/param/prerender2": { prerender: false },
diff --git a/test/tests.ts b/test/tests.ts
index 7fe4dae579..8967e26140 100644
--- a/test/tests.ts
+++ b/test/tests.ts
@@ -394,6 +394,12 @@ export function testNitro(
       "x-content-type-options": "nosniff",
       "x-frame-options": "DENY",
     });
+
+    const { data } = await callHandler({
+      url: "/api/error?custom_error_handler",
+    });
+    expect(status).toBe(503);
+    expect(data).toBe("custom_error_handler");
   });
 
   it.skipIf(isWindows && ctx.preset === "nitro-dev")(