--- a/browser/components/extensions/ext-windows.js
+++ b/browser/components/extensions/ext-windows.js
@@ -34,22 +34,26 @@ extensions.registerSchemaAPI("windows", 
         fire(WindowManager.getId(window));
       }).api(),
 
       onFocusChanged: new EventManager(context, "windows.onFocusChanged", fire => {
         // Keep track of the last windowId used to fire an onFocusChanged event
         let lastOnFocusChangedWindowId;
 
         let listener = event => {
-          let window = WindowManager.topWindow;
-          let windowId = window ? WindowManager.getId(window) : WindowManager.WINDOW_ID_NONE;
-          if (windowId !== lastOnFocusChangedWindowId) {
-            fire(windowId);
-            lastOnFocusChangedWindowId = windowId;
-          }
+          // Wait a tick to avoid firing a superfluous WINDOW_ID_NONE
+          // event when switching focus between two Firefox windows.
+          Promise.resolve().then(() => {
+            let window = Services.focus.activeWindow;
+            let windowId = window ? WindowManager.getId(window) : WindowManager.WINDOW_ID_NONE;
+            if (windowId !== lastOnFocusChangedWindowId) {
+              fire(windowId);
+              lastOnFocusChangedWindowId = windowId;
+            }
+          });
         };
         AllWindowEvents.addListener("focus", listener);
         AllWindowEvents.addListener("blur", listener);
         return () => {
           AllWindowEvents.removeListener("focus", listener);
           AllWindowEvents.removeListener("blur", listener);
         };
       }).api(),

--- a/browser/components/extensions/test/browser/browser_ext_windows_events.js
+++ b/browser/components/extensions/test/browser/browser_ext_windows_events.js
@@ -11,20 +11,25 @@ add_task(function* testWindowsEvents() {
 
       browser.test.assertTrue(Number.isInteger(window.id),
                               "Window object's id is an integer");
       browser.test.assertEq("normal", window.type,
                             "Window object returned with the correct type");
       browser.test.sendMessage("window-created", window.id);
     });
 
-    let lastWindowId;
+    let lastWindowId, os;
     browser.windows.onFocusChanged.addListener(function listener(windowId) {
       browser.test.log(`onFocusChange: windowId=${windowId} lastWindowId=${lastWindowId}`);
 
+      if (windowId === browser.windows.WINDOW_ID_NONE && os === "linux") {
+        browser.test.log("Ignoring a superfluous WINDOW_ID_NONE (blur) event on Linux");
+        return;
+      }
+
       browser.test.assertTrue(lastWindowId !== windowId,
                               "onFocusChanged fired once for the given window");
       lastWindowId = windowId;
 
       browser.test.assertTrue(Number.isInteger(windowId),
                               "windowId is an integer");
 
       browser.windows.getLastFocused().then(window => {
@@ -38,17 +43,20 @@ add_task(function* testWindowsEvents() {
       browser.test.log(`onRemoved: windowId=${windowId}`);
 
       browser.test.assertTrue(Number.isInteger(windowId),
                               "windowId is an integer");
       browser.test.sendMessage(`window-removed`, windowId);
       browser.test.notifyPass("windows.events");
     });
 
-    browser.test.sendMessage("ready");
+    browser.runtime.getPlatformInfo(info => {
+      os = info.os;
+      browser.test.sendMessage("ready");
+    });
   }
 
   let extension = ExtensionTestUtils.loadExtension({
     background: `(${background})()`,
   });
 
   yield extension.startup();
   yield extension.awaitMessage("ready");