diff --git a/desktop/flipper-server/package.json b/desktop/flipper-server/package.json
index 0cf31e80a..a8e6d4a28 100644
--- a/desktop/flipper-server/package.json
+++ b/desktop/flipper-server/package.json
@@ -10,12 +10,15 @@
   "bugs": "https://github.com/facebook/flipper/issues",
   "dependenciesComment": "mac-ca is required dynamically for darwin, node-fetch is treated special in electron-requires, not sure why",
   "dependencies": {
+    "http-proxy": "^1.18.1",
     "mac-ca": "^1.0.6",
     "node-fetch": "^2.6.7",
-    "ws": "^8.5.0"
+    "ws": "^8.5.0",
+    "xdg-basedir": "^4"
   },
   "devDependencies": {
     "@types/express": "^4.17.13",
+    "@types/http-proxy": "^1.17.8",
     "@types/node": "^15.12.5",
     "chalk": "^4.1.2",
     "express": "^4.17.3",
diff --git a/desktop/flipper-server/src/startBaseServer.tsx b/desktop/flipper-server/src/startBaseServer.tsx
index 1f115d06e..3101a8b9c 100644
--- a/desktop/flipper-server/src/startBaseServer.tsx
+++ b/desktop/flipper-server/src/startBaseServer.tsx
@@ -7,6 +7,7 @@
  * @format
  */
 
+import os from 'os';
 import express, {Express} from 'express';
 import http from 'http';
 import path from 'path';
@@ -14,6 +15,10 @@ import fs from 'fs-extra';
 import {VerifyClientCallbackSync, WebSocketServer} from 'ws';
 import {WEBSOCKET_MAX_MESSAGE_SIZE} from 'flipper-server-core';
 import {parse} from 'url';
+import xdgBasedir from 'xdg-basedir';
+import proxy from 'http-proxy';
+
+import {userInfo} from 'os';
 
 type Config = {
   port: number;
@@ -26,7 +31,7 @@ export async function startBaseServer(config: Config): Promise<{
   server: http.Server;
   socket: WebSocketServer;
 }> {
-  const {app, server} = await startAssetServer(config);
+  const {app, server} = await startHTTPServer(config);
   const socket = addWebsocket(server, config);
   return {
     app,
@@ -35,7 +40,7 @@ export async function startBaseServer(config: Config): Promise<{
   };
 }
 
-function startAssetServer(
+async function startHTTPServer(
   config: Config,
 ): Promise<{app: Express; server: http.Server}> {
   const app = express();
@@ -59,10 +64,41 @@ function startAssetServer(
 
   app.use(express.static(config.staticDir));
 
+  return startProxyServer(config, app);
+}
+
+async function startProxyServer(
+  config: Config,
+  app: Express,
+): Promise<{app: Express; server: http.Server}> {
   const server = http.createServer(app);
 
+  // For now, we only support domain socket access on POSIX-like systems.
+  if (os.platform() === 'win32') {
+    return new Promise((resolve) => {
+      console.log(`Starting server on http://localhost:${config.port}`);
+      server.listen(config.port, undefined, () => resolve({app, server}));
+    });
+  }
+
+  const runtimeDir = xdgBasedir.runtime || '/tmp';
+  await fs.mkdirp(runtimeDir);
+  const socketPath = `${runtimeDir}/flipper-server-${userInfo().uid}.sock`;
+
+  // TODO: More careful cleanup.
+  await fs.rm(socketPath, {force: true});
+
+  const proxyServer = proxy.createProxyServer({
+    target: {host: 'localhost', port: 0, socketPath},
+    autoRewrite: true,
+    ws: true,
+  });
+  console.log('Starting socket server on ', socketPath);
+  console.log(`Starting proxy server on http://localhost:${config.port}`);
+
   return new Promise((resolve) => {
-    server.listen(config.port, undefined, () => resolve({app, server}));
+    proxyServer.listen(config.port);
+    server.listen(socketPath, undefined, () => resolve({app, server}));
   });
 }
 
diff --git a/desktop/flipper-server/src/startSocketServer.tsx b/desktop/flipper-server/src/startSocketServer.tsx
index 6cd2a102c..9d18fd144 100644
--- a/desktop/flipper-server/src/startSocketServer.tsx
+++ b/desktop/flipper-server/src/startSocketServer.tsx
@@ -23,9 +23,12 @@ export function startSocketServer(
   socket: WebSocketServer,
 ) {
   socket.on('connection', (client, req) => {
-    const clientAddress = `${req.socket.remoteAddress}:${req.socket.remotePort}`;
+    const clientAddress =
+      (req.socket.remoteAddress &&
+        ` ${req.socket.remoteAddress}:${req.socket.remotePort}`) ||
+      '';
 
-    console.log(chalk.green(`Client connected ${clientAddress}`));
+    console.log(chalk.green(`Client connected${clientAddress}`));
 
     let connected = true;
 
diff --git a/desktop/yarn.lock b/desktop/yarn.lock
index 8b428eedf..b9e8a79b2 100644
--- a/desktop/yarn.lock
+++ b/desktop/yarn.lock
@@ -2504,6 +2504,13 @@
     "@types/react" "*"
     hoist-non-react-statics "^3.3.0"
 
+"@types/http-proxy@^1.17.8":
+  version "1.17.8"
+  resolved "https://registry.yarnpkg.com/@types/http-proxy/-/http-proxy-1.17.8.tgz#968c66903e7e42b483608030ee85800f22d03f55"
+  integrity sha512-5kPLG5BKpWYkw/LVOGWpiq3nEVqxiN32rTgI53Sk12/xHFQ2rG3ehI9IO+O3W2QoKeyB92dJkoka8SUm6BX1pA==
+  dependencies:
+    "@types/node" "*"
+
 "@types/inquirer@^7.3.3":
   version "7.3.3"
   resolved "https://registry.yarnpkg.com/@types/inquirer/-/inquirer-7.3.3.tgz#92e6676efb67fa6925c69a2ee638f67a822952ac"
@@ -5925,7 +5932,7 @@ event-target-shim@^5.0.0:
   resolved "https://registry.yarnpkg.com/event-target-shim/-/event-target-shim-5.0.1.tgz#5d4d3ebdf9583d63a5333ce2deb7480ab2b05789"
   integrity sha512-i/2XbnSz/uxRCU6+NdVJgKWDTM427+MqYbkQzD321DuCQJUqOuJKIA0IM2+W2xtYHdKOmZ4dR6fExsd4SXL+WQ==
 
-eventemitter3@^4.0.7:
+eventemitter3@^4.0.0, eventemitter3@^4.0.7:
   version "4.0.7"
   resolved "https://registry.yarnpkg.com/eventemitter3/-/eventemitter3-4.0.7.tgz#2de9b68f6528d5644ef5c59526a1b4a07306169f"
   integrity sha512-8guHBZCwKnFhYdHr2ysuRWErTwhoN2X8XELRlrRwpmfeY2jjuUN4taQMsULKUVo1K4DvZl+0pgfyoysHxvmvEw==
@@ -6351,6 +6358,11 @@ follow-redirects@1.5.10:
   dependencies:
     debug "=3.1.0"
 
+follow-redirects@^1.0.0:
+  version "1.14.9"
+  resolved "https://registry.yarnpkg.com/follow-redirects/-/follow-redirects-1.14.9.tgz#dd4ea157de7bfaf9ea9b3fbd85aa16951f78d8d7"
+  integrity sha512-MQDfihBQYMcyy5dhRDJUHcw7lb2Pv/TuE6xP1vyraLukNDHKbDxDNaOE3NbCAdKQApno+GPRyo1YAp89yCjK4w==
+
 follow-redirects@^1.14.8:
   version "1.14.8"
   resolved "https://registry.yarnpkg.com/follow-redirects/-/follow-redirects-1.14.8.tgz#016996fb9a11a100566398b1c6839337d7bfa8fc"
@@ -6882,6 +6894,15 @@ http-proxy-agent@^5.0.0:
     agent-base "6"
     debug "4"
 
+http-proxy@^1.18.1:
+  version "1.18.1"
+  resolved "https://registry.yarnpkg.com/http-proxy/-/http-proxy-1.18.1.tgz#401541f0534884bbf95260334e72f88ee3976549"
+  integrity sha512-7mz/721AbnJwIVbnaSv1Cz3Am0ZLT/UBwkC92VlxhXv/k/BBQfM2fXElQNC27BVGr0uwUpplYPQM9LnaBMR5NQ==
+  dependencies:
+    eventemitter3 "^4.0.0"
+    follow-redirects "^1.0.0"
+    requires-port "^1.0.0"
+
 https-proxy-agent@^5.0.0:
   version "5.0.0"
   resolved "https://registry.yarnpkg.com/https-proxy-agent/-/https-proxy-agent-5.0.0.tgz#e2a90542abb68a762e0a0850f6c9edadfd8506b2"
@@ -10806,6 +10827,11 @@ requireindex@~1.1.0:
   resolved "https://registry.yarnpkg.com/requireindex/-/requireindex-1.1.0.tgz#e5404b81557ef75db6e49c5a72004893fe03e162"
   integrity sha1-5UBLgVV+91225JxacgBIk/4D4WI=
 
+requires-port@^1.0.0:
+  version "1.0.0"
+  resolved "https://registry.yarnpkg.com/requires-port/-/requires-port-1.0.0.tgz#925d2601d39ac485e091cf0da5c6e694dc3dcaff"
+  integrity sha1-kl0mAdOaxIXgkc8NpcbmlNw9yv8=
+
 reselect@^4.1.5:
   version "4.1.5"
   resolved "https://registry.yarnpkg.com/reselect/-/reselect-4.1.5.tgz#852c361247198da6756d07d9296c2b51eddb79f6"
@@ -12637,7 +12663,7 @@ ws@~8.2.3:
   resolved "https://registry.yarnpkg.com/ws/-/ws-8.2.3.tgz#63a56456db1b04367d0b721a0b80cae6d8becbba"
   integrity sha512-wBuoj1BDpC6ZQ1B7DWQBYVLphPWkm8i9Y0/3YdHjHKHiohOJ1ws+3OccDWtH+PoC9DZD5WOTrJvNbWvjS6JWaA==
 
-xdg-basedir@^4.0.0:
+xdg-basedir@^4, xdg-basedir@^4.0.0:
   version "4.0.0"
   resolved "https://registry.yarnpkg.com/xdg-basedir/-/xdg-basedir-4.0.0.tgz#4bc8d9984403696225ef83a1573cbbcb4e79db13"
   integrity sha512-PSNhEJDejZYV7h50BohL09Er9VaIefr2LMAf3OEmpCkjOi34eYyQYAXUTjEQtZJTKcF0E2UKTh+osDLsgNim9Q==