diff --git a/packages/utils/network.ts b/packages/utils/network.ts
index de32b45d7f840..5f721242eb277 100644
--- a/packages/utils/network.ts
+++ b/packages/utils/network.ts
@@ -59,6 +59,10 @@ export function httpRequest(params: HTTPRequestParams, onResponse: (r: http.Inco
     const parsedProxyURL = normalizeProxyURL(proxyURL);
     if (params.url.startsWith('http:')) {
       options.path = url.toString();
+      const headers = options.headers || {};
+      if (!Object.keys(headers).some(header => header.toLowerCase() === 'host'))
+        headers.host = url.host;
+      options.headers = headers;
       url = parsedProxyURL;
     } else {
       options.agent = new HttpsProxyAgent(parsedProxyURL);
diff --git a/tests/config/proxy.ts b/tests/config/proxy.ts
index 697f39f956dff..1e534268dfc04 100644
--- a/tests/config/proxy.ts
+++ b/tests/config/proxy.ts
@@ -38,6 +38,7 @@ export class TestProxy {
 
   connectHosts: string[] = [];
   requestUrls: string[] = [];
+  requestHosts: string[] = [];
   wsUrls: string[] = [];
 
   private readonly _server: ProxyServer;
@@ -69,6 +70,7 @@ export class TestProxy {
   forwardTo(port: number, options?: { allowConnectRequests?: boolean, removePrefix?: string, preserveHostname?: boolean }) {
     this._prependHandler('request', (req: IncomingMessage) => {
       this.requestUrls.push(req.url);
+      this.requestHosts.push(req.headers.host);
       const url = new URL(req.url, `http://${req.headers.host}`);
       if (options?.preserveHostname)
         url.port = '' + port;
@@ -116,6 +118,7 @@ export class TestProxy {
   reset() {
     this.connectHosts = [];
     this.requestUrls = [];
+    this.requestHosts = [];
     for (const { event, handler } of this._handlers)
       this._server.removeListener(event, handler);
     this._handlers = [];
diff --git a/tests/library/chromium/connect-over-cdp.spec.ts b/tests/library/chromium/connect-over-cdp.spec.ts
index f68634fa55e0c..889f0b35f88a4 100644
--- a/tests/library/chromium/connect-over-cdp.spec.ts
+++ b/tests/library/chromium/connect-over-cdp.spec.ts
@@ -448,6 +448,25 @@ test('should use env proxy with connectOverCDP discovery request', async ({ brow
   }
 });
 
+test('should send target Host header when using env HTTP proxy with connectOverCDP', async ({ browserType, server, proxyServer, mode }) => {
+  test.info().annotations.push({ type: 'issue', description: 'https://github.com/microsoft/playwright/issues/40811' });
+  test.skip(mode !== 'default'); // Out of process transport does not allow us to set env vars dynamically.
+  proxyServer.forwardTo(server.PORT);
+
+  const oldValue = process.env.HTTP_PROXY;
+  try {
+    process.env.HTTP_PROXY = proxyServer.URL;
+    const error = await browserType.connectOverCDP(server.PREFIX).catch(e => e);
+    expect(error.message).toContain(`Unexpected status 404 when connecting to ${server.PREFIX}/json/version/`);
+    expect(proxyServer.requestHosts).toEqual([new URL(server.PREFIX).host]);
+  } finally {
+    if (oldValue === undefined)
+      delete process.env.HTTP_PROXY;
+    else
+      process.env.HTTP_PROXY = oldValue;
+  }
+});
+
 test('should be able to connect via localhost', async ({ browserType }, testInfo) => {
   const port = 9339 + testInfo.workerIndex;
   const browserServer = await browserType.launch({