diff --git a/browser/devtools/debugger/debugger-controller.js b/browser/devtools/debugger/debugger-controller.js
index 059152a5e8c6..bb305252a36c 100644
--- a/browser/devtools/debugger/debugger-controller.js
+++ b/browser/devtools/debugger/debugger-controller.js
@@ -123,6 +123,7 @@ let DebuggerController = {
     this._remoteConnectionTimeout = window.setTimeout(function() {
       // If we couldn't connect to any server yet, try again...
       if (!DebuggerController.activeThread) {
+        DebuggerController._onRemoteConnectionTimeout();
         DebuggerController._connect();
       }
     }, Prefs.remoteTimeout);
@@ -130,6 +131,14 @@ let DebuggerController = {
     return true;
   },
 
+  /**
+   * Called when a remote connection timeout occurs.
+   */
+  _onRemoteConnectionTimeout: function DC__onRemoteConnectionTimeout() {
+    Cu.reportError("Couldn't connect to " +
+      Prefs.remoteHost + ":" + Prefs.remotePort);
+  },
+
   /**
    * Initializes a debugger client and connects it to the debugger server,
    * wiring event handlers as necessary.
diff --git a/browser/devtools/debugger/test/browser_dbg_createRemote.js b/browser/devtools/debugger/test/browser_dbg_createRemote.js
index 261cccbc7753..13cca8fd786d 100644
--- a/browser/devtools/debugger/test/browser_dbg_createRemote.js
+++ b/browser/devtools/debugger/test/browser_dbg_createRemote.js
@@ -7,6 +7,7 @@
 
 var gWindow = null;
 var gTab = null;
+var gRemotePort = null;
 var gAutoConnect = null;
 
 const TEST_URL = EXAMPLE_URL + "browser_dbg_iframes.html";
@@ -17,6 +18,11 @@ function test() {
     gWindow = aWindow;
     let gDebugger = gWindow.contentWindow;
 
+    info("Current remote port: " +
+      Services.prefs.getIntPref("devtools.debugger.remote-port"));
+    info("Current autoconnect flag: " +
+      Services.prefs.getBoolPref("devtools.debugger.remote-autoconnect"));
+
     is(gDebugger.document.getElementById("close").getAttribute("hidden"), "true",
       "The close button should be hidden in a remote debugger.");
 
@@ -60,21 +66,46 @@ function test() {
     }
     DebuggerServer.closeListener();
 
+    gRemotePort = Services.prefs.getIntPref("devtools.debugger.remote-port");
     gAutoConnect = Services.prefs.getBoolPref("devtools.debugger.remote-autoconnect");
-    Services.prefs.setBoolPref("devtools.debugger.remote-autoconnect", true);
 
     // Open the listener at some point in the future to test automatic reconnect.
-    window.setTimeout(function() {
-      DebuggerServer.openListener(
-        Services.prefs.getIntPref("devtools.debugger.remote-port"));
-    }, Math.random() * 1000);
+    openListener(gRemotePort + 1);
   });
 }
 
+let attempts = 0;
+
+function openListener(port) {
+  Services.prefs.setIntPref("devtools.debugger.remote-port", port);
+  Services.prefs.setBoolPref("devtools.debugger.remote-autoconnect", true);
+
+  info("Attempting to open a new listener on port " + port);
+  try {
+    info("Closing listener...");
+    DebuggerServer.closeListener();
+    info("Opening listener...");
+    DebuggerServer.openListener(port);
+  } catch (e) {
+    info(e);
+    info("Exception caught when opening listener on port " + port);
+    info("Retrying with port " + (++port));
+
+    if (++attempts < 100) {
+      DebuggerServer.closeListener();
+      openListener(port);
+    } else {
+      ok(false, "Timed out while opening a listener.");
+    }
+  }
+}
+
 registerCleanupFunction(function() {
+  Services.prefs.setIntPref("devtools.debugger.remote-port", gRemotePort);
   Services.prefs.setBoolPref("devtools.debugger.remote-autoconnect", gAutoConnect);
   removeTab(gTab);
   gWindow = null;
   gTab = null;
+  gRemotePort = null;
   gAutoConnect = null;
 });