diff --git a/netwerk/cache/nsCacheService.cpp b/netwerk/cache/nsCacheService.cpp
index a83a3e23292b..1915f23ab89c 100644
--- a/netwerk/cache/nsCacheService.cpp
+++ b/netwerk/cache/nsCacheService.cpp
@@ -1588,6 +1588,7 @@ nsCacheService::GetCustomOfflineDevice(nsIFile *aProfileDir,
         rv = CreateCustomOfflineDevice(aProfileDir, aQuota, aDevice);
         NS_ENSURE_SUCCESS(rv, rv);
 
+        (*aDevice)->SetAutoShutdown();
         mCustomOfflineDevices.Put(profilePath, *aDevice);
     }
 
@@ -1676,6 +1677,20 @@ nsCacheService::CreateMemoryDevice()
     return rv;
 }
 
+nsresult
+nsCacheService::RemoveCustomOfflineDevice(nsOfflineCacheDevice *aDevice)
+{
+    nsCOMPtr<nsIFile> profileDir = aDevice->BaseDirectory();
+    if (!profileDir)
+        return NS_ERROR_UNEXPECTED;
+
+    nsAutoString profilePath;
+    nsresult rv = profileDir->GetPath(profilePath);
+    NS_ENSURE_SUCCESS(rv, rv);
+
+    mCustomOfflineDevices.Remove(profilePath);
+    return NS_OK;
+}
 
 nsresult
 nsCacheService::CreateRequest(nsCacheSession *   session,
diff --git a/netwerk/cache/nsCacheService.h b/netwerk/cache/nsCacheService.h
index ae4dcdcf8f39..5ec8abbed27a 100644
--- a/netwerk/cache/nsCacheService.h
+++ b/netwerk/cache/nsCacheService.h
@@ -199,6 +199,8 @@ private:
                                                nsOfflineCacheDevice **aDevice);
     nsresult         CreateMemoryDevice();
 
+    nsresult         RemoveCustomOfflineDevice(nsOfflineCacheDevice *aDevice);
+
     nsresult         CreateRequest(nsCacheSession *   session,
                                    const nsACString & clientKey,
                                    nsCacheAccessMode  accessRequested,
diff --git a/netwerk/cache/nsDiskCacheDeviceSQL.cpp b/netwerk/cache/nsDiskCacheDeviceSQL.cpp
index 08bd8cbb69f0..fdafabe2b932 100644
--- a/netwerk/cache/nsDiskCacheDeviceSQL.cpp
+++ b/netwerk/cache/nsDiskCacheDeviceSQL.cpp
@@ -685,6 +685,10 @@ nsApplicationCache::Activate()
   NS_ENSURE_TRUE(mDevice, NS_ERROR_NOT_AVAILABLE);
 
   mDevice->ActivateCache(mGroup, mClientID);
+
+  if (mDevice->AutoShutdown(this))
+    mDevice = nsnull;
+
   return NS_OK;
 }
 
@@ -830,6 +834,7 @@ nsOfflineCacheDevice::nsOfflineCacheDevice()
   : mDB(nsnull)
   , mCacheCapacity(0)
   , mDeltaCounter(0)
+  , mAutoShutdown(false)
 {
 }
 
@@ -2418,3 +2423,23 @@ nsOfflineCacheDevice::SetCapacity(PRUint32 capacity)
 {
   mCacheCapacity = capacity * 1024;
 }
+
+bool
+nsOfflineCacheDevice::AutoShutdown(nsIApplicationCache * aAppCache)
+{
+  if (!mAutoShutdown)
+    return false;
+
+  mAutoShutdown = false;
+
+  Shutdown();
+
+  nsRefPtr<nsCacheService> cacheService = nsCacheService::GlobalInstance();
+  cacheService->RemoveCustomOfflineDevice(this);
+
+  nsCAutoString clientID;
+  aAppCache->GetClientID(clientID);
+  mCaches.Remove(clientID);
+
+  return true;
+}
diff --git a/netwerk/cache/nsDiskCacheDeviceSQL.h b/netwerk/cache/nsDiskCacheDeviceSQL.h
index 25d311924d58..1c76fa42dddc 100644
--- a/netwerk/cache/nsDiskCacheDeviceSQL.h
+++ b/netwerk/cache/nsDiskCacheDeviceSQL.h
@@ -167,6 +167,8 @@ public:
 
   void                    SetCacheParentDirectory(nsIFile * parentDir);
   void                    SetCapacity(PRUint32  capacity);
+  void                    SetAutoShutdown() { mAutoShutdown = true; }
+  bool                    AutoShutdown(nsIApplicationCache * aAppCache);
 
   nsIFile *               BaseDirectory() { return mBaseDirectory; }
   nsIFile *               CacheDirectory() { return mCacheDirectory; }
@@ -257,6 +259,7 @@ private:
   nsCOMPtr<nsIFile>               mCacheDirectory;
   PRUint32                        mCacheCapacity; // in bytes
   PRInt32                         mDeltaCounter;
+  bool                            mAutoShutdown;
 
   nsInterfaceHashtable<nsCStringHashKey, nsIWeakReference> mCaches;
   nsClassHashtable<nsCStringHashKey, nsCString> mActiveCachesByGroup;
diff --git a/netwerk/test/unit/test_cacheForOfflineUse_no-store.js b/netwerk/test/unit/test_cacheForOfflineUse_no-store.js
index a0dad53763bf..303c2b4d1cff 100644
--- a/netwerk/test/unit/test_cacheForOfflineUse_no-store.js
+++ b/netwerk/test/unit/test_cacheForOfflineUse_no-store.js
@@ -5,7 +5,7 @@ do_load_httpd_js();
 
 var httpServer = null;
 const testFileName = "test_nsHttpChannel_CacheForOfflineUse-no-store";
-const cacheClientID = testFileName;
+const cacheClientID = testFileName + "|fake-group-id";
 const basePath = "/" + testFileName + "/";
 const baseURI = "http://localhost:4444" + basePath;
 const normalEntry = "normal";
@@ -17,9 +17,13 @@ function make_channel_for_offline_use(url, callback, ctx) {
   var ios = Cc["@mozilla.org/network/io-service;1"].
             getService(Ci.nsIIOService);
   var chan = ios.newChannel(url, "", null);
-  var cachingChan = chan.QueryInterface(Ci.nsICachingChannel);
-  cachingChan.cacheForOfflineUse = true;
-  cachingChan.offlineCacheClientID = cacheClientID;
+  
+  var cacheService = Components.classes["@mozilla.org/network/application-cache-service;1"].
+                     getService(Components.interfaces.nsIApplicationCacheService);
+  var appCache = cacheService.getApplicationCache(cacheClientID);
+  
+  var appCacheChan = chan.QueryInterface(Ci.nsIApplicationCacheChannel);
+  appCacheChan.applicationCacheForWrite = appCache;
   return chan;
 }
 
diff --git a/netwerk/test/unit/test_offlinecache_custom-directory.js b/netwerk/test/unit/test_offlinecache_custom-directory.js
index 43becb2a2e8e..52c6921f9ec5 100644
--- a/netwerk/test/unit/test_offlinecache_custom-directory.js
+++ b/netwerk/test/unit/test_offlinecache_custom-directory.js
@@ -64,6 +64,22 @@ function finish_test(customDir)
   file2.append("0B457F75198B29-0");
   do_check_eq(file2.exists(), true);
 
+  // This must not throw an exception.  After the update has finished
+  // the index file can be freely removed.  This way we check this process
+  // is no longer keeping the file open.  Check like this will probably
+  // work only Windows systems.
+
+  // This test could potentially randomaly fail when we start closing
+  // the offline cache database off the main thread.  Tries in a loop
+  // may be a solution then.
+  try {
+    indexSqlFile.remove(false);
+    do_check_true(true);
+  }
+  catch (ex) {
+    do_throw("Could not remove the sqlite.index file, we still keep it open \n" + ex + "\n");
+  }
+
   httpServer.stop(do_test_finished);
 }