diff --git a/src/dev/server.ts b/src/dev/server.ts
index a6b5e33d87..aedd770275 100644
--- a/src/dev/server.ts
+++ b/src/dev/server.ts
@@ -18,6 +18,8 @@ import { isTest, isCI } from "std-env";
 import { NitroDevApp } from "./app.ts";
 import { writeDevBuildInfo } from "../build/info.ts";
 
+const SHUTDOWN_TIMEOUT = 5000;
+
 export function createDevServer(nitro: Nitro): NitroDevServer {
   return new NitroDevServer(nitro);
 }
@@ -34,6 +36,8 @@ export class NitroDevServer extends NitroDevApp implements RunnerRPCHooks {
   #building?: boolean = true; // Assume initial build will start soon
   #buildError?: unknown;
   #reloadPromise?: Promise<void>;
+  #shuttingDown: boolean = false;
+  #closing: boolean = false;
 
   constructor(nitro: Nitro) {
     super(nitro, async (event) => {
@@ -76,6 +80,9 @@ export class NitroDevServer extends NitroDevApp implements RunnerRPCHooks {
       });
     });
     this.#manager.onClose((_runner, cause) => {
+      if (this.#shuttingDown) {
+        return;
+      }
       this.#workerError = cause;
       if (this.#workerRetries++ < 3) {
         this.nitro.logger.info("Restarting dev worker...", cause ? `Cause: ${cause}` : "");
@@ -146,6 +153,9 @@ export class NitroDevServer extends NitroDevApp implements RunnerRPCHooks {
   }
 
   async close() {
+    this.#closing = true;
+    await this.#reloadPromise?.catch(() => {});
+    await this.#shutdownWorker();
     await Promise.all(
       [
         Promise.all(this.#listeners.map((l) => l.close())).then(() => {
@@ -164,6 +174,9 @@ export class NitroDevServer extends NitroDevApp implements RunnerRPCHooks {
   }
 
   reload() {
+    if (this.#closing) {
+      return;
+    }
     const nextReload = (this.#reloadPromise ?? Promise.resolve())
       .catch(() => {})
       .then(() => this.#reload());
@@ -175,6 +188,7 @@ export class NitroDevServer extends NitroDevApp implements RunnerRPCHooks {
   }
 
   async #reload() {
+    await this.#shutdownWorker();
     const runnerName =
       this.nitro.options.devServer.runner || process.env.NITRO_DEV_RUNNER || "node-worker";
     const runner = await loadRunner(runnerName as RunnerName, {
@@ -200,6 +214,42 @@ export class NitroDevServer extends NitroDevApp implements RunnerRPCHooks {
 
   // #region Private Methods
 
+  async #shutdownWorker() {
+    if (!this.#manager.ready) {
+      return;
+    }
+    this.#shuttingDown = true;
+    try {
+      await new Promise<void>((resolve) => {
+        const done = () => {
+          clearTimeout(timer);
+          this.#manager.offMessage(listener);
+          resolve();
+        };
+        const timer = setTimeout(() => {
+          this.nitro.logger.warn("Dev worker did not shut down in time, force closing it...");
+          done();
+        }, SHUTDOWN_TIMEOUT);
+        const listener = (message: any) => {
+          if (message?.event === "exit") {
+            done();
+          }
+        };
+        this.#manager.onMessage(listener);
+        try {
+          this.#manager.sendMessage({ event: "shutdown" });
+        } catch (error) {
+          this.nitro.logger.warn(
+            `Could not send shutdown message to the dev worker: ${error instanceof Error ? error.message : String(error)}`
+          );
+          done();
+        }
+      });
+    } finally {
+      this.#shuttingDown = false;
+    }
+  }
+
   async #waitForBuild() {
     const timeout = isTest || isCI ? 60_000 : 6000;
     await this.#manager.waitForReady(timeout);