diff --git a/server/src/server.js b/server/src/server.js
index 3501400ea..0e4420ba9 100644
--- a/server/src/server.js
+++ b/server/src/server.js
@@ -1,136 +1,155 @@
 // @flow
 
 import cluster from 'cluster';
 import cookieParser from 'cookie-parser';
 import express from 'express';
 import expressWs from 'express-ws';
 import os from 'os';
 
 import './cron/cron';
 import { migrate } from './database/migrations';
 import { jsonEndpoints } from './endpoints';
 import { emailSubscriptionResponder } from './responders/comm-landing-responders';
 import {
   jsonHandler,
   httpGetHandler,
   downloadHandler,
   htmlHandler,
   uploadHandler,
 } from './responders/handlers';
 import landingHandler from './responders/landing-handler';
 import { errorReportDownloadResponder } from './responders/report-responders';
 import {
   createNewVersionResponder,
   markVersionDeployedResponder,
 } from './responders/version-responders';
 import { websiteResponder } from './responders/website-responders';
 import { onConnection } from './socket/socket';
 import {
   multerProcessor,
   multimediaUploadResponder,
   uploadDownloadResponder,
 } from './uploads/uploads';
-import { getGlobalURLFacts, getLandingURLFacts } from './utils/urls';
+import {
+  getGlobalURLFacts,
+  getLandingURLFacts,
+  generateAllRoutePaths,
+  generateBaseAndCommAppRoutePaths,
+} from './utils/urls';
 
 const { baseRoutePath } = getGlobalURLFacts();
 const landingBaseRoutePath = getLandingURLFacts().baseRoutePath;
 
 if (cluster.isMaster) {
   (async () => {
     const didMigrationsSucceed: boolean = await migrate();
     if (!didMigrationsSucceed) {
       // The following line uses exit code 2 to ensure nodemon exits
       // in a dev environment, instead of restarting. Context provided
       // in https://github.com/remy/nodemon/issues/751
       process.exit(2);
     }
     const cpuCount = os.cpus().length;
     for (let i = 0; i < cpuCount; i++) {
       cluster.fork();
     }
   })();
   cluster.on('exit', () => cluster.fork());
 } else {
   const server = express();
   expressWs(server);
   server.use(express.json({ limit: '50mb' }));
   server.use(cookieParser());
 
   const router = express.Router();
-  router.use('/images', express.static('images'));
-  router.use(`${landingBaseRoutePath}images`, express.static('images'));
-  router.use('/fonts', express.static('fonts'));
-  router.use(`${landingBaseRoutePath}fonts`, express.static('fonts'));
-  router.use('/misc', express.static('misc'));
+  for (const routePath of generateAllRoutePaths('images')) {
+    router.use(routePath, express.static('images'));
+  }
+  for (const routePath of generateAllRoutePaths('fonts')) {
+    router.use(routePath, express.static('fonts'));
+  }
+  for (const routePath of generateBaseAndCommAppRoutePaths('misc')) {
+    router.use(routePath, express.static('misc'));
+  }
   router.use(
     '/.well-known',
     express.static(
       '.well-known',
       // Necessary for apple-app-site-association file
       {
         setHeaders: res => res.setHeader('Content-Type', 'application/json'),
       },
     ),
   );
   const compiledFolderOptions =
     process.env.NODE_ENV === 'development'
       ? undefined
       : { maxAge: '1y', immutable: true };
-  router.use(
-    '/compiled',
-    express.static('app_compiled', compiledFolderOptions),
-  );
+  for (const routePath of generateBaseAndCommAppRoutePaths('compiled')) {
+    router.use(
+      routePath,
+      express.static('app_compiled', compiledFolderOptions),
+    );
+  }
   router.use(
     `${landingBaseRoutePath}compiled`,
     express.static('landing_compiled', compiledFolderOptions),
   );
-  router.use('/', express.static('icons'));
-  router.use('/commlanding', express.static('landing_icons'));
+  for (const routePath of generateBaseAndCommAppRoutePaths('')) {
+    router.use(routePath, express.static('icons'));
+  }
+  router.use(`${landingBaseRoutePath}`, express.static('landing_icons'));
 
   for (const endpoint in jsonEndpoints) {
     // $FlowFixMe Flow thinks endpoint is string
     const responder = jsonEndpoints[endpoint];
     const expectCookieInvalidation = endpoint === 'log_out';
-    router.post(
-      `/${endpoint}`,
-      jsonHandler(responder, expectCookieInvalidation),
-    );
+    for (const routePath of generateBaseAndCommAppRoutePaths(endpoint)) {
+      router.post(routePath, jsonHandler(responder, expectCookieInvalidation));
+    }
   }
 
   router.post(
     `${landingBaseRoutePath}subscribe_email`,
     emailSubscriptionResponder,
   );
 
-  router.get(
-    '/create_version/:deviceType/:codeVersion',
-    httpGetHandler(createNewVersionResponder),
-  );
-  router.get(
-    '/mark_version_deployed/:deviceType/:codeVersion',
-    httpGetHandler(markVersionDeployedResponder),
-  );
-
-  router.get(
-    '/download_error_report/:reportID',
-    downloadHandler(errorReportDownloadResponder),
-  );
-  router.get(
-    '/upload/:uploadID/:secret',
-    downloadHandler(uploadDownloadResponder),
-  );
+  for (const routePath of generateBaseAndCommAppRoutePaths(
+    'create_version/:deviceType/:codeVersion',
+  )) {
+    router.get(routePath, httpGetHandler(createNewVersionResponder));
+  }
+  for (const routePath of generateBaseAndCommAppRoutePaths(
+    'mark_version_deployed/:deviceType/:codeVersion',
+  )) {
+    router.get(routePath, httpGetHandler(markVersionDeployedResponder));
+  }
+  for (const routePath of generateBaseAndCommAppRoutePaths(
+    'download_error_report/:reportID',
+  )) {
+    router.get(routePath, downloadHandler(errorReportDownloadResponder));
+  }
+  for (const routePath of generateBaseAndCommAppRoutePaths(
+    'upload/:uploadID/:secret',
+  )) {
+    router.get(routePath, downloadHandler(uploadDownloadResponder));
+  }
 
   // $FlowFixMe express-ws has side effects that can't be typed
-  router.ws('/ws', onConnection);
+  router.ws(`${baseRoutePath}ws`, onConnection);
   router.get(`${landingBaseRoutePath}*`, landingHandler);
   router.get('*', htmlHandler(websiteResponder));
 
-  router.post(
-    '/upload_multimedia',
-    multerProcessor,
-    uploadHandler(multimediaUploadResponder),
-  );
+  for (const routePath of generateBaseAndCommAppRoutePaths(
+    'upload_multimedia',
+  )) {
+    router.post(
+      routePath,
+      multerProcessor,
+      uploadHandler(multimediaUploadResponder),
+    );
+  }
 
   server.use(baseRoutePath, router);
   server.listen(parseInt(process.env.PORT, 10) || 3000, 'localhost');
 }
diff --git a/server/src/utils/urls.js b/server/src/utils/urls.js
index 6ab8df9fd..b005d66eb 100644
--- a/server/src/utils/urls.js
+++ b/server/src/utils/urls.js
@@ -1,51 +1,66 @@
 // @flow
 
 import commAppURLFacts from '../../facts/commapp_url';
 import landingURLFacts from '../../facts/landing_url';
 import squadCalURLFacts from '../../facts/squadcal_url';
 import baseURLFacts from '../../facts/url';
 
 type GlobalURLFacts = {
   +baseRoutePath: string,
 };
 
 function getGlobalURLFacts(): GlobalURLFacts {
   return baseURLFacts;
 }
 
 export type AppURLFacts = {
   +baseDomain: string,
   +basePath: string,
   +https: boolean,
 };
 type LandingURLFacts = {
   ...AppURLFacts,
   +baseRoutePath: string,
 };
 
 function getSquadCalURLFacts(): AppURLFacts {
   return squadCalURLFacts;
 }
 
 function getCommAppURLFacts(): AppURLFacts {
   return commAppURLFacts;
 }
 
 function getAppURLFactsFromRequestURL(url: string): AppURLFacts {
   const commURLFacts = getCommAppURLFacts();
   return url.startsWith(commURLFacts.basePath)
     ? commURLFacts
     : getSquadCalURLFacts();
 }
 
 function getLandingURLFacts(): LandingURLFacts {
   return landingURLFacts;
 }
 
+function generateAllRoutePaths(endpoint: string): string[] {
+  const landingBaseRoutePath = landingURLFacts.baseRoutePath;
+  const routePaths = generateBaseAndCommAppRoutePaths(endpoint);
+  routePaths.push(landingBaseRoutePath + endpoint);
+  return routePaths;
+}
+
+function generateBaseAndCommAppRoutePaths(endpoint: string): string[] {
+  const { baseRoutePath } = baseURLFacts;
+  const commAppBaseRoutePath = commAppURLFacts.basePath;
+  return [baseRoutePath + endpoint, commAppBaseRoutePath + endpoint];
+}
+
 export {
   getGlobalURLFacts,
   getSquadCalURLFacts,
   getCommAppURLFacts,
   getLandingURLFacts,
   getAppURLFactsFromRequestURL,
+  generateAllRoutePaths,
+  generateBaseAndCommAppRoutePaths,
 };