diff --git a/.changeset/fix-websocket-econnreset.md b/.changeset/fix-websocket-econnreset.md
new file mode 100644
index 000000000000..b1f7474c1b32
--- /dev/null
+++ b/.changeset/fix-websocket-econnreset.md
@@ -0,0 +1,7 @@
+---
+"@cloudflare/vite-plugin": patch
+---
+
+Fix dev server crash on WebSocket client disconnect
+
+When a WebSocket client disconnects while an upgrade request is being processed, the server would crash with an unhandled `ECONNRESET` error. The fix adds an error handler to the socket at the start of the upgrade process.
diff --git a/packages/vite-plugin-cloudflare/src/__tests__/websockets.spec.ts b/packages/vite-plugin-cloudflare/src/__tests__/websockets.spec.ts
new file mode 100644
index 000000000000..3294045f48f7
--- /dev/null
+++ b/packages/vite-plugin-cloudflare/src/__tests__/websockets.spec.ts
@@ -0,0 +1,65 @@
+import http from "node:http";
+import net from "node:net";
+import { DeferredPromise, Miniflare, Response } from "miniflare";
+import { afterEach, beforeEach, describe, expect, test, vi } from "vitest";
+import { handleWebSocket } from "../websockets";
+import type { AddressInfo } from "node:net";
+
+describe("handleWebSocket", () => {
+	let httpServer: http.Server;
+	let miniflare: Miniflare;
+	let port: number;
+
+	beforeEach(async () => {
+		httpServer = http.createServer((_req, res) => res.end("OK"));
+		miniflare = new Miniflare({
+			modules: true,
+			script: `export default {
+				fetch() {
+					const [client, server] = Object.values(new WebSocketPair());
+					server.accept();
+					return new Response(null, { status: 101, webSocket: client });
+				}
+			}`,
+		});
+		handleWebSocket(httpServer, miniflare);
+		await new Promise<void>((r) => httpServer.listen(0, "127.0.0.1", r));
+		port = (httpServer.address() as AddressInfo).port;
+	});
+
+	afterEach(async () => {
+		await miniflare?.dispose();
+		await new Promise<void>((resolve, reject) =>
+			httpServer?.close((e) => (e ? reject(e) : resolve()))
+		);
+	});
+
+	// https://github.com/cloudflare/workers-sdk/issues/12047
+	test("survives client disconnect during upgrade", async () => {
+		// Mock dispatchFetch to simulate a slow response - the bug occurs when
+		// the client disconnects while dispatchFetch is pending
+		const deferred = new DeferredPromise<Response>();
+		vi.spyOn(miniflare, "dispatchFetch").mockReturnValue(deferred);
+
+		const socket = net.connect(port, "127.0.0.1");
+		await new Promise<void>((r) => socket.on("connect", r));
+		socket.write(
+			"GET / HTTP/1.1\r\n" +
+				"Host: localhost\r\n" +
+				"Upgrade: websocket\r\n" +
+				"Connection: Upgrade\r\n" +
+				"Sec-WebSocket-Key: dGhlIHNhbXBsZSBub25jZQ==\r\n" +
+				"Sec-WebSocket-Version: 13\r\n\r\n"
+		);
+
+		// Reset connection while dispatchFetch is pending, triggering ECONNRESET
+		socket.resetAndDestroy();
+
+		// Resolve the mock so miniflare.dispose() doesn't hang in afterEach
+		deferred.resolve(new Response(null));
+
+		// Verify server did not crash and is still responsive
+		const response = await fetch(`http://127.0.0.1:${port}`);
+		expect(response.ok).toBe(true);
+	});
+});
diff --git a/packages/vite-plugin-cloudflare/src/websockets.ts b/packages/vite-plugin-cloudflare/src/websockets.ts
index a984ea25b12f..5d1a959cd0df 100644
--- a/packages/vite-plugin-cloudflare/src/websockets.ts
+++ b/packages/vite-plugin-cloudflare/src/websockets.ts
@@ -20,6 +20,9 @@ export function handleWebSocket(
 	httpServer.on(
 		"upgrade",
 		async (request: IncomingMessage, socket: Duplex, head: Buffer) => {
+			// Socket errors crash Node.js if unhandled
+			socket.on("error", () => socket.destroy());
+
 			const url = new URL(request.url ?? "", UNKNOWN_HOST);
 
 			// Ignore Vite HMR WebSockets