diff --git a/packages/react-dev-utils/WebpackDevServerUtils.js b/packages/react-dev-utils/WebpackDevServerUtils.js
index 1208d7fc776..260f73ceea0 100644
--- a/packages/react-dev-utils/WebpackDevServerUtils.js
+++ b/packages/react-dev-utils/WebpackDevServerUtils.js
@@ -34,20 +34,20 @@ if (isSmokeTest) {
   };
 }
 
-function prepareUrls(protocol, host, port) {
+function prepareUrls(protocol, host, port, pathname) {
   const formatUrl = hostname =>
     url.format({
       protocol,
       hostname,
       port,
-      pathname: '/',
+      pathname,
     });
   const prettyPrintUrl = hostname =>
     url.format({
       protocol,
       hostname,
       port: chalk.bold(port),
-      pathname: '/',
+      pathname,
     });
 
   const isUnspecifiedHost = host === '0.0.0.0' || host === '::';
diff --git a/packages/react-dev-utils/errorOverlayMiddleware.js b/packages/react-dev-utils/errorOverlayMiddleware.js
index 873b1994732..57a6003e45d 100644
--- a/packages/react-dev-utils/errorOverlayMiddleware.js
+++ b/packages/react-dev-utils/errorOverlayMiddleware.js
@@ -9,9 +9,9 @@
 const launchEditor = require('./launchEditor');
 const launchEditorEndpoint = require('./launchEditorEndpoint');
 
-module.exports = function createLaunchEditorMiddleware() {
+module.exports = function createLaunchEditorMiddleware(servedPathPathname) {
   return function launchEditorMiddleware(req, res, next) {
-    if (req.url.startsWith(launchEditorEndpoint)) {
+    if (req.url.startsWith(`${servedPathPathname}${launchEditorEndpoint}`)) {
       const lineNumber = parseInt(req.query.lineNumber, 10) || 1;
       const colNumber = parseInt(req.query.colNumber, 10) || 1;
       launchEditor(req.query.fileName, lineNumber, colNumber);
diff --git a/packages/react-dev-utils/noopServiceWorkerMiddleware.js b/packages/react-dev-utils/noopServiceWorkerMiddleware.js
index 568ff4d6519..ad32c09b230 100644
--- a/packages/react-dev-utils/noopServiceWorkerMiddleware.js
+++ b/packages/react-dev-utils/noopServiceWorkerMiddleware.js
@@ -7,9 +7,11 @@
 
 'use strict';
 
-module.exports = function createNoopServiceWorkerMiddleware() {
+module.exports = function createNoopServiceWorkerMiddleware(
+  servedPathPathname
+) {
   return function noopServiceWorkerMiddleware(req, res, next) {
-    if (req.url === '/service-worker.js') {
+    if (req.url === `${servedPathPathname}/service-worker.js`) {
       res.setHeader('Content-Type', 'text/javascript');
       res.send(
         `// This service worker file is effectively a 'no-op' that will reset any
diff --git a/packages/react-dev-utils/package.json b/packages/react-dev-utils/package.json
index 48197f822c3..8f40e19955e 100644
--- a/packages/react-dev-utils/package.json
+++ b/packages/react-dev-utils/package.json
@@ -16,6 +16,7 @@
     "clearConsole.js",
     "crossSpawn.js",
     "errorOverlayMiddleware.js",
+    "serveAppMiddleware.js",
     "eslintFormatter.js",
     "FileSizeReporter.js",
     "formatWebpackMessages.js",
diff --git a/packages/react-dev-utils/serveAppMiddleware.js b/packages/react-dev-utils/serveAppMiddleware.js
new file mode 100644
index 00000000000..c2824a96d32
--- /dev/null
+++ b/packages/react-dev-utils/serveAppMiddleware.js
@@ -0,0 +1,21 @@
+/**
+ * Copyright (c) 2015-present, Facebook, Inc.
+ *
+ * This source code is licensed under the MIT license found in the
+ * LICENSE file in the root directory of this source tree.
+ */
+'use strict';
+
+module.exports = function createServeAppMiddleware(servedPathPathname) {
+  return function serveAppMiddleware(req, res, next) {
+    if (servedPathPathname.length > 1 && servedPathPathname !== './') {
+      if (req.url.indexOf(servedPathPathname) === -1) {
+        res.redirect(servedPathPathname);
+      } else {
+        next();
+      }
+    } else {
+      next();
+    }
+  };
+};
diff --git a/packages/react-scripts/config/webpack.config.dev.js b/packages/react-scripts/config/webpack.config.dev.js
index 7a1b66803bc..8bf6ea2bac5 100644
--- a/packages/react-scripts/config/webpack.config.dev.js
+++ b/packages/react-scripts/config/webpack.config.dev.js
@@ -10,6 +10,7 @@
 
 const autoprefixer = require('autoprefixer');
 const path = require('path');
+const url = require('url');
 const webpack = require('webpack');
 const HtmlWebpackPlugin = require('html-webpack-plugin');
 const CaseSensitivePathsPlugin = require('case-sensitive-paths-webpack-plugin');
@@ -22,14 +23,18 @@ const getClientEnvironment = require('./env');
 const paths = require('./paths');
 
 // Webpack uses `publicPath` to determine where the app is being served from.
-// In development, we always serve from the root. This makes config easier.
-const publicPath = '/';
+// In development, we serve from the root by default. Webpack will serve from
+// the relative path of the homepage field if specified.
+let publicPath = url.parse(paths.servedPath).pathname || '';
+if (publicPath === './') {
+  publicPath = publicPath.slice(1);
+}
 // `publicUrl` is just like `publicPath`, but we will provide it to our app
 // as %PUBLIC_URL% in `index.html` and `process.env.PUBLIC_URL` in JavaScript.
 // Omit trailing slash as %PUBLIC_PATH%/xyz looks better than %PUBLIC_PATH%xyz.
-const publicUrl = '';
+const publicUrl = paths.servedPath.slice(0, -1) + '/static';
 // Get environment variables to inject into our app.
-const env = getClientEnvironment(publicUrl);
+const env = getClientEnvironment(publicUrl === '.' ? '' : publicUrl);
 
 // Options for PostCSS as we reference these options twice
 // Adds vendor prefixing based on your specified browser support in
@@ -111,6 +116,7 @@ module.exports = {
     // There are also additional JS chunk files if you use code splitting.
     chunkFilename: 'static/js/[name].chunk.js',
     // This is the URL that app is served from. We use "/" in development.
+    // If there is a homepage path defined, it will be served from that instead.
     publicPath: publicPath,
     // Point sourcemap entries to original disk location (format as URL on Windows)
     devtoolModuleFilenameTemplate: info =>
diff --git a/packages/react-scripts/config/webpackDevServer.config.js b/packages/react-scripts/config/webpackDevServer.config.js
index 74119d27f39..69fe86d8448 100644
--- a/packages/react-scripts/config/webpackDevServer.config.js
+++ b/packages/react-scripts/config/webpackDevServer.config.js
@@ -10,12 +10,16 @@
 
 const errorOverlayMiddleware = require('react-dev-utils/errorOverlayMiddleware');
 const noopServiceWorkerMiddleware = require('react-dev-utils/noopServiceWorkerMiddleware');
+const serveAppMiddleware = require('react-dev-utils/serveAppMiddleware');
 const ignoredFiles = require('react-dev-utils/ignoredFiles');
+const url = require('url');
 const config = require('./webpack.config.dev');
 const paths = require('./paths');
+const express = require('express');
 
 const protocol = process.env.HTTPS === 'true' ? 'https' : 'http';
 const host = process.env.HOST || '0.0.0.0';
+const servedPathPathname = url.parse(paths.servedPath).pathname || '';
 
 module.exports = function(proxy, allowedHost) {
   return {
@@ -86,18 +90,26 @@ module.exports = function(proxy, allowedHost) {
       // Paths with dots should still use the history fallback.
       // See https://github.com/facebook/create-react-app/issues/387.
       disableDotRule: true,
+      index: servedPathPathname,
     },
     public: allowedHost,
     proxy,
     before(app) {
       // This lets us open files from the runtime error overlay.
-      app.use(errorOverlayMiddleware());
+      app.use(errorOverlayMiddleware(servedPathPathname));
       // This service worker file is effectively a 'no-op' that will reset any
       // previous service worker registered for the same host:port combination.
       // We do this in development to avoid hitting the production cache if
       // it used the same host and port.
       // https://github.com/facebook/create-react-app/issues/2272#issuecomment-302832432
-      app.use(noopServiceWorkerMiddleware());
+      app.use(noopServiceWorkerMiddleware(servedPathPathname));
+      // serves the app up from the homepage if specified
+      app.use(serveAppMiddleware(servedPathPathname));
+      // serve up static assets
+      app.use(
+        `${config.output.publicPath.slice(0, -1)}/static`,
+        express.static(paths.appPublic)
+      );
     },
   };
 };
diff --git a/packages/react-scripts/fixtures/kitchensink/integration/env.test.js b/packages/react-scripts/fixtures/kitchensink/integration/env.test.js
index 43badcbde8e..ee7f27c383f 100644
--- a/packages/react-scripts/fixtures/kitchensink/integration/env.test.js
+++ b/packages/react-scripts/fixtures/kitchensink/integration/env.test.js
@@ -50,7 +50,7 @@ describe('Integration', () => {
 
       const prefix =
         process.env.NODE_ENV === 'development'
-          ? ''
+          ? '/static'
           : 'http://www.example.org/spa';
       expect(doc.getElementById('feature-public-url').textContent).to.equal(
         `${prefix}.`
diff --git a/packages/react-scripts/scripts/start.js b/packages/react-scripts/scripts/start.js
index 95502bc2a24..127cc4b4c92 100644
--- a/packages/react-scripts/scripts/start.js
+++ b/packages/react-scripts/scripts/start.js
@@ -29,6 +29,7 @@ if (process.env.SKIP_PREFLIGHT_CHECK !== 'true') {
 }
 // @remove-on-eject-end
 
+const url = require('url');
 const chalk = require('chalk');
 const webpack = require('webpack');
 const WebpackDevServer = require('webpack-dev-server');
@@ -56,6 +57,8 @@ if (!checkRequiredFiles([paths.appHtml, paths.appIndexJs])) {
 const DEFAULT_PORT = parseInt(process.env.PORT, 10) || 3000;
 const HOST = process.env.HOST || '0.0.0.0';
 
+const servedPathPathname = url.parse(paths.servedPath).pathname || '';
+
 if (process.env.HOST) {
   console.log(
     chalk.cyan(
@@ -89,7 +92,7 @@ checkBrowsers(paths.appPath)
     }
     const protocol = process.env.HTTPS === 'true' ? 'https' : 'http';
     const appName = require(paths.appPackageJson).name;
-    const urls = prepareUrls(protocol, HOST, port);
+    const urls = prepareUrls(protocol, HOST, port, servedPathPathname);
     // Create a webpack compiler that is configured with custom messages.
     const compiler = createCompiler(
       webpack,
diff --git a/packages/react-scripts/template/README.md b/packages/react-scripts/template/README.md
index 21cf719e961..c30d9031817 100644
--- a/packages/react-scripts/template/README.md
+++ b/packages/react-scripts/template/README.md
@@ -2192,6 +2192,13 @@ To override this, specify the `homepage` in your `package.json`, for example:
 
 This will let Create React App correctly infer the root path to use in the generated HTML file.
 
+If `homepage` is specified, Create React App will open your browser at the path specified. From the example above, `npm start` would result in:
+
+```js
+http://localhost:3000/relativepath
+```
+This also means that in development the paths to the static files will be served out of the `relativepath` directory.
+
 **Note**: If you are using `react-router@^4`, you can root `<Link>`s using the `basename` prop on any `<Router>`.<br>
 More information [here](https://reacttraining.com/react-router/web/api/BrowserRouter/basename-string).<br>
 <br>