diff --git a/toolkit/components/enterprisepolicies/EnterprisePolicies.js b/toolkit/components/enterprisepolicies/EnterprisePolicies.js
index 45378909622c..9ef6fa193131 100644
--- a/toolkit/components/enterprisepolicies/EnterprisePolicies.js
+++ b/toolkit/components/enterprisepolicies/EnterprisePolicies.js
@@ -23,6 +23,9 @@ XPCOMUtils.defineLazyModuleGetters(this, {
 // ${InstallDir}/distribution folder.
 const POLICIES_FILENAME = "policies.json";
 
+// When true browser policy is loaded per-user from
+// /run/user/$UID/appname
+const PREF_PER_USER_DIR = "toolkit.policies.perUserDir";
 // For easy testing, modify the helpers/sample.json file,
 // and set PREF_ALTERNATE_PATH in firefox.js as:
 // /your/repo/browser/components/enterprisepolicies/helpers/sample.json
@@ -455,7 +458,12 @@ class JSONPoliciesProvider {
   _getConfigurationFile() {
     let configFile = null;
     try {
-      configFile = Services.dirsvc.get("XREAppDist", Ci.nsIFile);
+      let perUserPath = Services.prefs.getBoolPref(PREF_PER_USER_DIR, false);
+      if (perUserPath) {
+        configFile = Services.dirsvc.get("XREUserRunTimeDir", Ci.nsIFile);
+      } else {
+        configFile = Services.dirsvc.get("XREAppDist", Ci.nsIFile);
+      }
       configFile.append(POLICIES_FILENAME);
     } catch (ex) {
       // Getting the correct directory will fail in xpcshell tests. This should
diff --git a/toolkit/xre/nsXREDirProvider.cpp b/toolkit/xre/nsXREDirProvider.cpp
index c3164f204ffd..979bd1484833 100644
--- a/toolkit/xre/nsXREDirProvider.cpp
+++ b/toolkit/xre/nsXREDirProvider.cpp
@@ -45,6 +45,7 @@
 #include "mozilla/Omnijar.h"
 #include "mozilla/Preferences.h"
 #include "mozilla/Telemetry.h"
+#include "nsPrintfCString.h"
 
 #include <stdlib.h>
 
@@ -103,7 +104,7 @@ nsCOMPtr<nsIFile> gDataDirProfile = nullptr;
 
 // These are required to allow nsXREDirProvider to be usable in xpcshell tests.
 // where gAppData is null.
-#if defined(XP_MACOSX) || defined(XP_WIN)
+#if defined(XP_MACOSX) || defined(XP_WIN) || defined(XP_UNIX)
 static const char* GetAppName() {
   if (gAppData) {
     return gAppData->name;
@@ -461,6 +462,14 @@ nsXREDirProvider::GetFile(const char* aProperty, bool* aPersistent,
 #endif
   } else if (!strcmp(aProperty, XRE_USER_SYS_EXTENSION_DEV_DIR)) {
     return GetSysUserExtensionsDevDirectory(aFile);
+  } else if (!strcmp(aProperty, XRE_USER_RUNTIME_DIR)) {
+#ifdef MOZ_WIDGET_GTK
+    nsPrintfCString path("/run/user/%d/%s/", getuid(), GetAppName());
+    ToLowerCase(path);
+    return NS_NewNativeLocalFile(path, false, aFile);
+#else
+    return NS_ERROR_FAILURE;
+#endif
   } else if (!strcmp(aProperty, XRE_APP_DISTRIBUTION_DIR)) {
     bool persistent = false;
     rv = GetFile(NS_GRE_DIR, &persistent, getter_AddRefs(file));
diff --git a/xpcom/build/nsXULAppAPI.h b/xpcom/build/nsXULAppAPI.h
index 121eb992812e..e1f0fd050472 100644
--- a/xpcom/build/nsXULAppAPI.h
+++ b/xpcom/build/nsXULAppAPI.h
@@ -141,6 +141,13 @@
  */
 #define XRE_ADDON_APP_DIR "XREAddonAppDir"
 
+/**
+ * A directory service key which specifies the distribution specific files for
+ * the application unique for each user.
+ * It's located at /run/user/$UID/<product name>/
+ */
+#define XRE_USER_RUNTIME_DIR "XREUserRunTimeDir"
+
 /**
  * A directory service key which provides the update directory. Callers should
  * fall back to appDir.