diff --git a/common/content/commandline.js b/common/content/commandline.js
index ceaab95d..3cf54785 100644
--- a/common/content/commandline.js
+++ b/common/content/commandline.js
@@ -623,10 +623,8 @@ var CommandLine = Module("commandline", {
             this.widgets.message = null;
         if (modes.main != modes.COMMAND_LINE)
             this.widgets.command = null;
-        if (modes.main == modes.OUTPUT_MULTILINE && this.widgets.multilineOutput.atEnd) {
-            dactyl.focusContent();
+        if (modes.main == modes.OUTPUT_MULTILINE && this.widgets.multilineOutput.atEnd)
             modes.pop();
-        }
         if (modes.main != modes.OUTPUT_MULTILINE)
             this.multilineOutputVisible = false;
     },
diff --git a/common/content/events.js b/common/content/events.js
index 666df991..0c3b5a7a 100644
--- a/common/content/events.js
+++ b/common/content/events.js
@@ -93,6 +93,7 @@ var Events = Module("events", {
         this._activeMenubar = false;
         this.addSessionListener(window, "DOMMenuBarActive", this.onDOMMenuBarActive, true);
         this.addSessionListener(window, "DOMMenuBarInactive", this.onDOMMenuBarInactive, true);
+        this.addSessionListener(window, "blur", this.onBlur, true);
         this.addSessionListener(window, "focus", this.onFocus, true);
         this.addSessionListener(window, "keydown", this.onKeyUpOrDown, true);
         this.addSessionListener(window, "keypress", this.onKeyPress, true);
@@ -724,6 +725,15 @@ var Events = Module("events", {
         }
     },
 
+    onBlur: function onFocus(event) {
+        if (event.originalTarget instanceof Window && services.focus.activeWindow == null)
+            // Deals with circumstances where, after the main window
+            // blurs while a collapsed frame has focus, re-activating
+            // the main window does not restore focus and we lose key
+            // input.
+            services.focus.clearFocus(window);
+    },
+
     // TODO: Merge with onFocusChange
     onFocus: function onFocus(event) {
         let elem = event.originalTarget;