diff --git a/browser/devtools/debugger/test/Makefile.in b/browser/devtools/debugger/test/Makefile.in
index 275083ae5cd2..de15fad53673 100644
--- a/browser/devtools/debugger/test/Makefile.in
+++ b/browser/devtools/debugger/test/Makefile.in
@@ -22,6 +22,7 @@ MOCHITEST_BROWSER_TESTS = \
 	browser_dbg_breakpoints-pane.js \
 	browser_dbg_chrome-debugging.js \
 	browser_dbg_clean-exit.js \
+	browser_dbg_clean-exit-window.js \
 	browser_dbg_cmd-blackbox.js \
 	browser_dbg_cmd-break.js \
 	browser_dbg_cmd-dbg.js \
diff --git a/browser/devtools/debugger/test/browser_dbg_clean-exit-window.js b/browser/devtools/debugger/test/browser_dbg_clean-exit-window.js
new file mode 100644
index 000000000000..aa0afc2acf0c
--- /dev/null
+++ b/browser/devtools/debugger/test/browser_dbg_clean-exit-window.js
@@ -0,0 +1,90 @@
+/* Any copyright is dedicated to the Public Domain.
+   http://creativecommons.org/publicdomain/zero/1.0/ */
+
+/**
+ * Test that closing a window with the debugger in a paused state exits cleanly.
+ */
+
+let gDebuggee, gPanel, gDebugger, gWindow;
+
+const TAB_URL = EXAMPLE_URL + "doc_inline-debugger-statement.html";
+
+function test() {
+  addWindow(TAB_URL)
+    .then(win => initDebugger(TAB_URL, win))
+    .then(([aTab, aDebuggee, aPanel, aWindow]) => {
+      gDebuggee = aDebuggee;
+      gPanel = aPanel;
+      gDebugger = gPanel.panelWin;
+      gWindow = aWindow;
+
+      return testCleanExit(gWindow);
+    })
+    .then(null, aError => {
+      ok(false, "Got an error: " + aError.message + "\n" + aError.stack);
+    });
+}
+
+function testCleanExit(aWindow) {
+  let deferred = promise.defer();
+
+  gWindow = aWindow;
+  ok(!!gWindow, "Second window created.");
+
+  gWindow.focus();
+
+  let topWindow = Services.wm.getMostRecentWindow("navigator:browser");
+  is(topWindow, gWindow,
+    "The second window is on top.");
+
+  let isActive = promise.defer();
+  let isLoaded = promise.defer();
+
+  promise.all([isActive.promise, isLoaded.promise]).then(() => {
+    gWindow.BrowserChromeTest.runWhenReady(() => {
+      waitForSourceAndCaretAndScopes(gPanel, ".html", 16).then(() => {
+        is(gDebugger.gThreadClient.paused, true,
+          "Should be paused after the debugger statement.");
+        gWindow.close();
+        deferred.resolve();
+        finish();
+      });
+
+      gDebuggee.runDebuggerStatement();
+    });
+  });
+
+  let focusManager = Cc["@mozilla.org/focus-manager;1"].getService(Ci.nsIFocusManager);
+  if (focusManager.activeWindow != gWindow) {
+    gWindow.addEventListener("activate", function onActivate(aEvent) {
+      if (aEvent.target != gWindow) {
+        return;
+      }
+      gWindow.removeEventListener("activate", onActivate, true);
+      isActive.resolve();
+    }, true);
+  } else {
+    isActive.resolve();
+  }
+
+  let contentLocation = gWindow.content.location.href;
+  if (contentLocation != TAB_URL) {
+    gWindow.document.addEventListener("load", function onLoad(aEvent) {
+      if (aEvent.target.documentURI != TAB_URL) {
+        return;
+      }
+      gWindow.document.removeEventListener("load", onLoad, true);
+      isLoaded.resolve();
+    }, true);
+  } else {
+    isLoaded.resolve();
+  }
+  return deferred.promise;
+}
+
+registerCleanupFunction(function() {
+  gWindow = null;
+  gDebuggee = null;
+  gPanel = null;
+  gDebugger = null;
+});
diff --git a/browser/devtools/debugger/test/head.js b/browser/devtools/debugger/test/head.js
index 2cfbc601d650..19c1582c8311 100644
--- a/browser/devtools/debugger/test/head.js
+++ b/browser/devtools/debugger/test/head.js
@@ -416,18 +416,18 @@ function backspaceText(aElement, aTimes) {
   }
 }
 
-function getTab(aTarget) {
+function getTab(aTarget, aWindow) {
   if (aTarget instanceof XULElement) {
     return promise.resolve(aTarget);
   } else {
-    return addTab(aTarget);
+    return addTab(aTarget, aWindow);
   }
 }
 
 function initDebugger(aTarget, aWindow) {
   info("Initializing a debugger panel.");
 
-  return getTab(aTarget).then(aTab => {
+  return getTab(aTarget, aWindow).then(aTab => {
     info("Debugee tab added successfully: " + aTarget);
 
     let deferred = promise.defer();
@@ -445,7 +445,7 @@ function initDebugger(aTarget, aWindow) {
         info("Debugger client resumed successfully.");
 
         prepareDebugger(debuggerPanel);
-        deferred.resolve([aTab, debuggee, debuggerPanel]);
+        deferred.resolve([aTab, debuggee, debuggerPanel, aWindow]);
       });
     });
 
diff --git a/toolkit/devtools/server/actors/script.js b/toolkit/devtools/server/actors/script.js
index 1d9b3692b235..0ae4530dcf6c 100644
--- a/toolkit/devtools/server/actors/script.js
+++ b/toolkit/devtools/server/actors/script.js
@@ -288,9 +288,17 @@ EventLoopStack.prototype = {
    * The URL of the debuggee who pushed the event loop on top of the stack.
    */
   get lastPausedUrl() {
-    return this.size > 0
-      ? this._inspector.lastNestRequestor.url
-      : null;
+    let url = null;
+    if (this.size > 0) {
+      try {
+        url = this._inspector.lastNestRequestor.url
+      } catch (e) {
+        // The tab's URL getter may throw if the tab is destroyed by the time
+        // this code runs, but we don't really care at this point.
+        dumpn(e);
+      }
+    }
+    return url;
   },
 
   /**
@@ -936,7 +944,7 @@ ThreadActor.prototype = {
     // In case of multiple nested event loops (due to multiple debuggers open in
     // different tabs or multiple debugger clients connected to the same tab)
     // only allow resumption in a LIFO order.
-    if (this._nestedEventLoops.size
+    if (this._nestedEventLoops.size && this._nestedEventLoops.lastPausedUrl
         && this._nestedEventLoops.lastPausedUrl !== this._hooks.url) {
       return {
         error: "wrongOrder",