diff --git a/layout/tools/reftest/reftest-cmdline.js b/layout/tools/reftest/reftest-cmdline.js
index c2a615c89ae..3b3b23b4724 100644
--- a/layout/tools/reftest/reftest-cmdline.js
+++ b/layout/tools/reftest/reftest-cmdline.js
@@ -110,8 +110,33 @@ RefTestCmdLineHandler.prototype =
 
     var wwatch = Components.classes["@mozilla.org/embedcomp/window-watcher;1"]
                            .getService(nsIWindowWatcher);
-    wwatch.openWindow(null, "chrome://reftest/content/reftest.xul", "_blank",
-                      "chrome,dialog=no,all", args);
+
+    function loadReftests() {
+      wwatch.openWindow(null, "chrome://reftest/content/reftest.xul", "_blank",
+                        "chrome,dialog=no,all", args);
+    }
+
+    var remote = false;
+    try {
+      remote = prefs.getBoolPref("reftest.remote");
+    } catch (ex) {
+    }
+
+    // If we are running on a remote machine, assume that we can't open another
+    // window for transferring focus to when tests don't require focus.
+    if (remote) {
+      loadReftests();
+    }
+    else {
+      // This dummy window exists solely for enforcing proper focus discipline.
+      var dummy = wwatch.openWindow(null, "about:blank", "dummy",
+                                    "chrome,dialog=no,left=800,height=200,width=200,all", null);
+      dummy.onload = function dummyOnload() {
+        dummy.focus();
+        loadReftests();
+      }
+    }
+
     cmdLine.preventDefault = true;
   },
 
diff --git a/layout/tools/reftest/reftest.js b/layout/tools/reftest/reftest.js
index 41305e0ccad..2a95b58889e 100644
--- a/layout/tools/reftest/reftest.js
+++ b/layout/tools/reftest/reftest.js
@@ -378,8 +378,10 @@ function InitAndStartRefTests()
         DoneTests();
     }
 
-    // Focus the content browser
-    gBrowser.focus();
+    // Focus the content browser.
+    if (gFocusFilterMode != FOCUS_FILTER_NON_NEEDS_FOCUS_TESTS) {
+        gBrowser.focus();
+    }
 
     StartTests();
 }
@@ -1118,6 +1120,15 @@ function Focus()
     return true;
 }
 
+function Blur()
+{
+    // On non-remote reftests, this will transfer focus to the dummy window
+    // we created to hold focus for non-needs-focus tests.  Buggy tests
+    // (ones which require focus but don't request needs-focus) will then
+    // fail.
+    gContainingWindow.blur();
+}
+
 function StartCurrentTest()
 {
     gTestLog = [];
@@ -1150,6 +1161,9 @@ function StartCurrentTest()
     }
     else {
         gDumpLog("REFTEST TEST-START | " + gURLs[0].prettyPath + "\n");
+        if (!gURLs[0].needsFocus) {
+            Blur();
+        }
         var currentTest = gTotalTests - gURLs.length;
         gContainingWindow.document.title = "reftest: " + currentTest + " / " + gTotalTests +
             " (" + Math.floor(100 * (currentTest / gTotalTests)) + "%)";