diff --git a/setup/start/nginx/nginx.conf b/setup/start/nginx/nginx.conf
index cd246b0b4..ce6803ab2 100644
--- a/setup/start/nginx/nginx.conf
+++ b/setup/start/nginx/nginx.conf
@@ -39,4 +39,5 @@ http {
     limit_req_zone $binary_remote_addr zone=admin_login:10m rate=10r/s; # 10 request a second
 
     include applications/*.conf;
+    include applications/*/*.conf;
 }
diff --git a/src/reverseproxy.js b/src/reverseproxy.js
index e7dde99fb..c7ecc7084 100644
--- a/src/reverseproxy.js
+++ b/src/reverseproxy.js
@@ -525,7 +525,7 @@ async function writeAppNginxConfig(app, vhost, type, certificatePath) {
     }
 
     const nginxConf = ejs.render(NGINX_APPCONFIG_EJS, data);
-    const filename = path.join(paths.NGINX_APPCONFIG_DIR, `${app.id}-${vhost.replace('*', '_')}.conf`);
+    const filename = path.join(paths.NGINX_APPCONFIG_DIR, app.id, `${vhost.replace('*', '_')}.conf`);
     debug(`writeAppNginxConfig: writing config for "${vhost}" to ${filename} with options ${JSON.stringify(data)}`);
     if (!safe.fs.writeFileSync(filename, nginxConf)) {
         debug(`Error creating nginx config for "${app.fqdn}" : ${safe.error.message}`);
@@ -538,6 +538,8 @@ async function writeAppConfigs(app) {
 
     const locations = apps.getLocationsSync(app);
 
+    if (!safe.fs.mkdirSync(path.join(paths.NGINX_APPCONFIG_DIR, app.id), { recursive: true })) throw new BoxError(BoxError.FS_ERROR, `Could not create nginx config directory: ${safe.error.message}`);
+
     for (const location of locations) {
         const certificatePath = await getCertificatePath(location.fqdn, location.domain);
         await writeAppNginxConfig(app, location.fqdn, location.type, certificatePath);
@@ -581,15 +583,7 @@ async function configureApp(app, auditSource) {
 async function unconfigureApp(app) {
     assert.strictEqual(typeof app, 'object');
 
-    const configFilenames = safe.fs.readdirSync(paths.NGINX_APPCONFIG_DIR);
-    if (!configFilenames) throw new BoxError(BoxError.FS_ERROR, `Error loading nginx config files: ${safe.error.message}`);
-
-    for (const filename of configFilenames) {
-        if (!filename.startsWith(app.id)) continue;
-
-        safe.fs.unlinkSync(path.join(paths.NGINX_APPCONFIG_DIR, filename));
-    }
-
+    if (!safe.fs.rmSync(path.join(paths.NGINX_APPCONFIG_DIR, app.id), { recursive: true, force: true })) throw new BoxError(BoxError.FS_ERROR, `Could not remove nginx config directory: ${safe.error.message}`);
     await reload();
 }
 
@@ -734,12 +728,15 @@ async function checkCerts(auditSource, progressCallback) {
 function removeAppConfigs() {
     const dashboardConfigFilename = `${settings.dashboardFqdn()}.conf`;
 
-    debug('removeAppConfigs: reomving nginx configs of apps');
+    debug('removeAppConfigs: removing app nginx configs');
 
     // remove all configs which are not the default or current dashboard
-    for (const appConfigFile of fs.readdirSync(paths.NGINX_APPCONFIG_DIR)) {
-        if (appConfigFile !== constants.NGINX_DEFAULT_CONFIG_FILE_NAME && appConfigFile !== dashboardConfigFilename) {
-            fs.unlinkSync(path.join(paths.NGINX_APPCONFIG_DIR, appConfigFile));
+    for (const entry of fs.readdirSync(paths.NGINX_APPCONFIG_DIR, { withFileTypes: true })) {
+        const fullPath = path.join(paths.NGINX_APPCONFIG_DIR, entry.name);
+        if (entry.isDirectory()) {
+            fs.rmSync(fullPath, { recursive: true, force: true });
+        } else if (entry.isFile() && entry.name !== constants.NGINX_DEFAULT_CONFIG_FILE_NAME && entry.name !== dashboardConfigFilename) {
+            fs.unlinkSync(fullPath);
         }
     }
 }