diff --git a/browser/components/loop/LoopRooms.jsm b/browser/components/loop/LoopRooms.jsm
index 8fdeb51750f..4490041a043 100644
--- a/browser/components/loop/LoopRooms.jsm
+++ b/browser/components/loop/LoopRooms.jsm
@@ -68,7 +68,7 @@ let LoopRoomsInternal = {
     }
 
     Task.spawn(function* () {
-      yield MozLoopService.register();
+      yield MozLoopService.promiseRegisteredWithServers();
 
       if (!gDirty) {
         callback(null, [...this.rooms.values()]);
diff --git a/browser/components/loop/MozLoopAPI.jsm b/browser/components/loop/MozLoopAPI.jsm
index fb386983eff..b64aea507bf 100644
--- a/browser/components/loop/MozLoopAPI.jsm
+++ b/browser/components/loop/MozLoopAPI.jsm
@@ -369,7 +369,7 @@ function injectLoopAPI(targetWindow) {
       value: function(callback) {
         // We translate from a promise to a callback, as we can't pass promises from
         // Promise.jsm across the priv versus unpriv boundary.
-        MozLoopService.register().then(() => {
+        MozLoopService.promiseRegisteredWithServers().then(() => {
           callback(null);
         }, err => {
           callback(cloneValueInto(err, targetWindow));
diff --git a/browser/components/loop/MozLoopService.jsm b/browser/components/loop/MozLoopService.jsm
index bff41176a4d..36990f7ec30 100644
--- a/browser/components/loop/MozLoopService.jsm
+++ b/browser/components/loop/MozLoopService.jsm
@@ -30,6 +30,7 @@ Cu.import("resource://gre/modules/XPCOMUtils.jsm");
 Cu.import("resource://gre/modules/Promise.jsm");
 Cu.import("resource://gre/modules/osfile.jsm", this);
 Cu.import("resource://gre/modules/Task.jsm");
+Cu.import("resource://gre/modules/Timer.jsm");
 Cu.import("resource://gre/modules/FxAccountsOAuthClient.jsm");
 
 Cu.importGlobalProperties(["URL"]);
@@ -111,7 +112,6 @@ function getJSONPref(aName) {
 let gRegisteredDeferred = null;
 let gHawkClient = null;
 let gLocalizedStrings = null;
-let gInitializeTimer = null;
 let gFxAEnabled = true;
 let gFxAOAuthClientPromise = null;
 let gFxAOAuthClient = null;
@@ -309,7 +309,7 @@ let MozLoopServiceInternal = {
 
   /**
    * Starts registration of Loop with the push server, and then will register
-   * with the Loop server. It will return early if already registered.
+   * with the Loop server as a GUEST. It will return early if already registered.
    *
    * @returns {Promise} a promise that is resolved with no params on completion, or
    *          rejected with an error code or string.
@@ -871,42 +871,17 @@ let MozLoopServiceInternal = {
 };
 Object.freeze(MozLoopServiceInternal);
 
+
 let gInitializeTimerFunc = (deferredInitialization) => {
   // Kick off the push notification service into registering after a timeout.
   // This ensures we're not doing too much straight after the browser's finished
   // starting up.
-  gInitializeTimer = Cc["@mozilla.org/timer;1"].createInstance(Ci.nsITimer);
-  gInitializeTimer.initWithCallback(Task.async(function* initializationCallback() {
-    yield MozLoopService.register().then(Task.async(function*() {
-      if (!MozLoopServiceInternal.fxAOAuthTokenData) {
-        log.debug("MozLoopService: Initialized without an already logged-in account");
-        deferredInitialization.resolve("initialized to guest status");
-        return;
-      }
 
-      log.debug("MozLoopService: Initializing with already logged-in account");
-      let registeredPromise =
-            MozLoopServiceInternal.registerWithLoopServer(
-              LOOP_SESSION_TYPE.FXA, {
-                calls: MozLoopServiceInternal.pushHandler.registeredChannels[MozLoopService.channelIDs.callsFxA],
-                rooms: MozLoopServiceInternal.pushHandler.registeredChannels[MozLoopService.channelIDs.roomsFxA]
-              });
-      registeredPromise.then(() => {
-        deferredInitialization.resolve("initialized to logged-in status");
-      }, error => {
-        log.debug("MozLoopService: error logging in using cached auth token");
-        MozLoopServiceInternal.setError("login", error);
-        deferredInitialization.reject("error logging in using cached auth token");
-      });
-    }), error => {
-      log.debug("MozLoopService: Failure of initial registration", error);
-      deferredInitialization.reject(error);
-    });
-    gInitializeTimer = null;
-  }),
-  MozLoopServiceInternal.initialRegistrationDelayMilliseconds, Ci.nsITimer.TYPE_ONE_SHOT);
+  setTimeout(MozLoopService.delayedInitialize.bind(MozLoopService, deferredInitialization),
+             MozLoopServiceInternal.initialRegistrationDelayMilliseconds);
 };
 
+
 /**
  * Public API
  */
@@ -962,13 +937,60 @@ this.MozLoopService = {
     let deferredInitialization = Promise.defer();
     gInitializeTimerFunc(deferredInitialization);
 
-    return deferredInitialization.promise.catch(error => {
+    return deferredInitialization.promise;
+  }),
+
+  /**
+   * The core of the initialization work that happens once the browser is ready
+   * (after a timer when called during startup).
+   *
+   * Can be called more than once (e.g. if the initial setup fails at some phase).
+   * @param {Deferred} deferredInitialization
+   */
+  delayedInitialize: Task.async(function*(deferredInitialization) {
+    // Set or clear an error depending on how deferredInitialization gets resolved.
+    // We do this first so that it can handle the early returns below.
+    let completedPromise = deferredInitialization.promise.then(result => {
+      MozLoopServiceInternal.clearError("initialization");
+      return result;
+    },
+    error => {
+      // If we get a non-object then setError was already called for a different error type.
       if (typeof(error) == "object") {
-        // This never gets cleared since there is no UI to recover. Only restarting will work.
         MozLoopServiceInternal.setError("initialization", error);
       }
-      throw error;
     });
+
+    try {
+      yield this.promiseRegisteredWithServers();
+    } catch (ex) {
+      log.debug("MozLoopService: Failure of initial registration", ex);
+      deferredInitialization.reject(ex);
+      yield completedPromise;
+      return;
+    }
+
+    if (!MozLoopServiceInternal.fxAOAuthTokenData) {
+      log.debug("MozLoopService: Initialized without an already logged-in account");
+      deferredInitialization.resolve("initialized to guest status");
+      yield completedPromise;
+      return;
+    }
+
+    log.debug("MozLoopService: Initializing with already logged-in account");
+    let pushURLs = {
+      calls: MozLoopServiceInternal.pushHandler.registeredChannels[this.channelIDs.callsFxA],
+      rooms: MozLoopServiceInternal.pushHandler.registeredChannels[this.channelIDs.roomsFxA]
+    };
+
+    MozLoopServiceInternal.registerWithLoopServer(LOOP_SESSION_TYPE.FXA, pushURLs).then(() => {
+      deferredInitialization.resolve("initialized to logged-in status");
+    }, error => {
+      log.debug("MozLoopService: error logging in using cached auth token");
+      MozLoopServiceInternal.setError("login", error);
+      deferredInitialization.reject("error logging in using cached auth token");
+    });
+    yield completedPromise;
   }),
 
   /**
@@ -1081,25 +1103,10 @@ this.MozLoopService = {
                                              Services.tm.mainThread);
   },
 
-
   /**
-   * Starts registration of Loop with the push server, and then will register
-   * with the Loop server. It will return early if already registered.
-   *
-   * @returns {Promise} a promise that is resolved with no params on completion, or
-   *          rejected with an error code or string.
+   * @see MozLoopServiceInternal.promiseRegisteredWithServers
    */
-  register: function() {
-    log.debug("registering");
-    // Don't do anything if loop is not enabled.
-    if (!Services.prefs.getBoolPref("loop.enabled")) {
-      throw new Error("Loop is not enabled");
-    }
-
-    if (Services.prefs.getBoolPref("loop.throttled")) {
-      throw new Error("Loop is disabled by the soft-start mechanism");
-    }
-
+  promiseRegisteredWithServers: function() {
     return MozLoopServiceInternal.promiseRegisteredWithServers();
   },
 
diff --git a/browser/components/loop/test/mochitest/browser_fxa_login.js b/browser/components/loop/test/mochitest/browser_fxa_login.js
index aa270271c72..088b06b16ce 100644
--- a/browser/components/loop/test/mochitest/browser_fxa_login.js
+++ b/browser/components/loop/test/mochitest/browser_fxa_login.js
@@ -253,7 +253,7 @@ add_task(function* basicAuthorizationAndRegistration() {
   mockPushHandler.registrationPushURL = "https://localhost/pushUrl/guest";
   // Notification observed due to the error being cleared upon successful registration.
   let statusChangedPromise = promiseObserverNotified("loop-status-changed");
-  yield MozLoopService.register();
+  yield MozLoopService.promiseRegisteredWithServers();
   yield statusChangedPromise;
 
   // Normally the same pushUrl would be registered but we change it in the test
@@ -318,7 +318,7 @@ add_task(function* loginWithParams401() {
     test_error: "params_401",
   };
   yield promiseOAuthParamsSetup(BASE_URL, params);
-  yield MozLoopService.register();
+  yield MozLoopService.promiseRegisteredWithServers();
 
   let loginPromise = MozLoopService.logInToFxA();
   yield loginPromise.then(tokenData => {
diff --git a/browser/components/loop/test/xpcshell/head.js b/browser/components/loop/test/xpcshell/head.js
index 06ec7703109..4dac56080f6 100644
--- a/browser/components/loop/test/xpcshell/head.js
+++ b/browser/components/loop/test/xpcshell/head.js
@@ -31,6 +31,11 @@ var loopServer;
 Services.prefs.setBoolPref("loop.enabled", true);
 Services.prefs.setBoolPref("loop.throttled", false);
 
+// Cleanup function for all tests
+do_register_cleanup(() => {
+  MozLoopService.errors.clear();
+});
+
 function setupFakeLoopServer() {
   loopServer = new HttpServer();
   loopServer.start(-1);
diff --git a/browser/components/loop/test/xpcshell/test_looprooms.js b/browser/components/loop/test/xpcshell/test_looprooms.js
index 19c1a0fd7c5..07ba1c42c12 100644
--- a/browser/components/loop/test/xpcshell/test_looprooms.js
+++ b/browser/components/loop/test/xpcshell/test_looprooms.js
@@ -135,7 +135,7 @@ const compareRooms = function(room1, room2) {
 };
 
 add_task(function* test_getAllRooms() {
-  yield MozLoopService.register(mockPushHandler);
+  yield MozLoopService.promiseRegisteredWithServers();
 
   let rooms = yield LoopRooms.promise("getAll");
   Assert.equal(rooms.length, 3);
@@ -145,7 +145,7 @@ add_task(function* test_getAllRooms() {
 });
 
 add_task(function* test_getRoom() {
-  yield MozLoopService.register(mockPushHandler);
+  yield MozLoopService.promiseRegisteredWithServers();
 
   let roomToken = "_nxD4V4FflQ";
   let room = yield LoopRooms.promise("get", roomToken);
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_busy.js b/browser/components/loop/test/xpcshell/test_loopservice_busy.js
index 00db71c670a..3b89b8fdb23 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_busy.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_busy.js
@@ -24,7 +24,7 @@ let msgHandler = function(msg) {
 add_test(function test_busy_2guest_calls() {
   actionReceived = false;
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     let opened = 0;
     Chat.open = function() {
       opened++;
@@ -47,7 +47,7 @@ add_test(function test_busy_2guest_calls() {
 add_test(function test_busy_1fxa_1guest_calls() {
   actionReceived = false;
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     let opened = 0;
     Chat.open = function() {
       opened++;
@@ -71,7 +71,7 @@ add_test(function test_busy_1fxa_1guest_calls() {
 add_test(function test_busy_2fxa_calls() {
   actionReceived = false;
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     let opened = 0;
     Chat.open = function() {
       opened++;
@@ -94,7 +94,7 @@ add_test(function test_busy_2fxa_calls() {
 add_test(function test_busy_1guest_1fxa_calls() {
   actionReceived = false;
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     let opened = 0;
     Chat.open = function() {
       opened++;
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_dnd.js b/browser/components/loop/test/xpcshell/test_loopservice_dnd.js
index 3530dff5032..130af0909c3 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_dnd.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_dnd.js
@@ -31,7 +31,7 @@ add_test(function test_set_do_not_disturb() {
 add_test(function test_do_not_disturb_disabled_should_open_chat_window() {
   MozLoopService.doNotDisturb = false;
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     let opened = false;
     Chat.open = function() {
       opened = true;
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_initialize.js b/browser/components/loop/test/xpcshell/test_loopservice_initialize.js
index bc4b6c6c2b7..636d12424e3 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_initialize.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_initialize.js
@@ -1,7 +1,7 @@
 /* Any copyright is dedicated to the Public Domain.
    http://creativecommons.org/publicdomain/zero/1.0/ */
 
-var startTimerCalled = false;
+let startTimerCalled = false;
 
 /**
  * Tests that registration doesn't happen when the expiry time is
@@ -23,7 +23,7 @@ add_task(function test_initialize_no_expiry() {
  */
 add_task(function test_initialize_expiry_past() {
   // Set time to be 2 seconds in the past.
-  var nowSeconds = Date.now() / 1000;
+  let nowSeconds = Date.now() / 1000;
   Services.prefs.setIntPref("loop.urlsExpiryTimeSeconds", nowSeconds - 2);
   startTimerCalled = false;
 
@@ -39,7 +39,7 @@ add_task(function test_initialize_expiry_past() {
  */
 add_task(function test_initialize_starts_timer() {
   // Set time to be 1 minute in the future
-  var nowSeconds = Date.now() / 1000;
+  let nowSeconds = Date.now() / 1000;
   Services.prefs.setIntPref("loop.urlsExpiryTimeSeconds", nowSeconds + 60);
   startTimerCalled = false;
 
@@ -49,8 +49,7 @@ add_task(function test_initialize_starts_timer() {
     "should start the timer when expiry time is in the future");
 });
 
-function run_test()
-{
+function run_test() {
   setupFakeLoopServer();
 
   // Override MozLoopService's initializeTimer, so that we can verify the timeout is called
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_notification.js b/browser/components/loop/test/xpcshell/test_loopservice_notification.js
index eb92fcdabd3..f4ad6556fde 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_notification.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_notification.js
@@ -10,7 +10,7 @@ let openChatOrig = Chat.open;
 add_test(function test_openChatWindow_on_notification() {
   Services.prefs.setCharPref("loop.seenToS", "unseen");
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     let opened = false;
     Chat.open = function() {
       opened = true;
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_registration.js b/browser/components/loop/test/xpcshell/test_loopservice_registration.js
index 960bbc73d92..e4a858f210e 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_registration.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_registration.js
@@ -17,7 +17,7 @@ Cu.import("resource://services-common/utils.js");
 add_test(function test_register_websocket_success_loop_server_fail() {
   mockPushHandler.registrationResult = "404";
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     do_throw("should not succeed when loop server registration fails");
   }, (err) => {
     // 404 is an expected failure indicated by the lack of route being set
@@ -49,7 +49,7 @@ add_test(function test_register_success() {
     response.processAsync();
     response.finish();
   });
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     run_next_test();
   }, err => {
     do_throw("shouldn't error on a successful request");
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_restart.js b/browser/components/loop/test/xpcshell/test_loopservice_restart.js
index 733b678997f..ee55abcf442 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_restart.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_restart.js
@@ -75,12 +75,17 @@ add_task(function test_initialize_with_invalid_fxa_token() {
                  "FXA pref should be cleared if token was invalid");
     Assert.equal(Services.prefs.getCharPref(LOOP_FXA_PROFILE_PREF), "",
                  "FXA profile pref should be cleared if token was invalid");
+    Assert.ok(MozLoopServiceInternal.errors.has("login"),
+              "Initialization error should have been reported to UI");
   });
 });
 
 add_task(function test_initialize_with_fxa_token() {
   Services.prefs.setCharPref(LOOP_FXA_PROFILE_PREF, FAKE_FXA_PROFILE);
   Services.prefs.setCharPref(LOOP_FXA_TOKEN_PREF, FAKE_FXA_TOKEN_DATA);
+
+  MozLoopService.errors.clear();
+
   loopServer.registerPathHandler("/registration", (request, response) => {
     response.setStatusLine(null, 200, "OK");
   });
@@ -90,6 +95,7 @@ add_task(function test_initialize_with_fxa_token() {
                  "FXA pref should still be set after initialization");
     Assert.equal(Services.prefs.getCharPref(LOOP_FXA_PROFILE_PREF), FAKE_FXA_PROFILE,
                  "FXA profile should still be set after initialization");
+    Assert.ok(!MozLoopServiceInternal.errors.has("login"), "Initialization error should not exist");
   });
 });
 
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_token_invalid.js b/browser/components/loop/test/xpcshell/test_loopservice_token_invalid.js
index 507776f170e..49592446d24 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_token_invalid.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_token_invalid.js
@@ -31,7 +31,7 @@ add_test(function test_registration_invalid_token() {
     response.finish();
   });
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     // Due to the way the time stamp checking code works in hawkclient, we expect a couple
     // of authorization requests before we reset the token.
     Assert.equal(authorizationAttempts, 2);
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_token_save.js b/browser/components/loop/test/xpcshell/test_loopservice_token_save.js
index e9ecfbbbe52..d54ac694217 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_token_save.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_token_save.js
@@ -16,7 +16,7 @@ add_test(function test_registration_returns_hawk_session_token() {
     response.finish();
   });
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     var hawkSessionPref;
     try {
       hawkSessionPref = Services.prefs.getCharPref("loop.hawk-session-token");
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_token_send.js b/browser/components/loop/test/xpcshell/test_loopservice_token_send.js
index 855ef7c1f8a..eb0881a1aaa 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_token_send.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_token_send.js
@@ -24,7 +24,7 @@ add_test(function test_registration_uses_hawk_session_token() {
     response.finish();
   });
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     run_next_test();
   }, err => {
     do_throw("shouldn't error on a succesful request");
diff --git a/browser/components/loop/test/xpcshell/test_loopservice_token_validation.js b/browser/components/loop/test/xpcshell/test_loopservice_token_validation.js
index db1edb69feb..ee121a96852 100644
--- a/browser/components/loop/test/xpcshell/test_loopservice_token_validation.js
+++ b/browser/components/loop/test/xpcshell/test_loopservice_token_validation.js
@@ -16,7 +16,7 @@ add_test(function test_registration_handles_bogus_hawk_token() {
     response.finish();
   });
 
-  MozLoopService.register().then(() => {
+  MozLoopService.promiseRegisteredWithServers().then(() => {
     do_throw("should not succeed with a bogus token");
   }, err => {