--- a/devtools/client/shared/test/browser_html_tooltip-03.js
+++ b/devtools/client/shared/test/browser_html_tooltip-03.js
@@ -12,83 +12,136 @@ const HTML_NS = "http://www.w3.org/1999/
 const TEST_URI = `data:text/xml;charset=UTF-8,<?xml version="1.0"?>
   <?xml-stylesheet href="chrome://global/skin/global.css"?>
   <?xml-stylesheet href="chrome://devtools/skin/common.css"?>
   <window xmlns="http://www.mozilla.org/keymaster/gatekeeper/there.is.only.xul"
    title="Tooltip test">
     <vbox flex="1">
       <hbox id="box1" flex="1">test1</hbox>
       <hbox id="box2" flex="1">test2</hbox>
-      <hbox id="box3" flex="1">test3</hbox>
+      <hbox id="box3" flex="1">
+        <textbox id="box3-input"></textbox>
+      </hbox>
       <hbox id="box4" flex="1">
         <textbox id="box4-input"></textbox>
       </hbox>
     </vbox>
   </window>`;
 
 const {HTMLTooltip} = require("devtools/client/shared/widgets/HTMLTooltip");
 loadHelperScript("helper_html_tooltip.js");
 
 add_task(function* () {
   yield addTab("about:blank");
   let [,, doc] = yield createHost("bottom", TEST_URI);
 
-  yield testTooltipWithAutoFocus(doc);
-  yield testTooltipWithoutAutoFocus(doc);
+  yield testNoAutoFocus(doc);
+  yield testAutoFocus(doc);
+  yield testAutoFocusPreservesFocusChange(doc);
 });
 
-function* testTooltipWithAutoFocus(doc) {
-  info("Test a tooltip with autofocus takes focus when displayed");
-  let textbox = doc.querySelector("textbox");
-
-  info("Focus a XUL textbox");
-  let onInputFocus = once(textbox, "focus");
-  EventUtils.synthesizeMouseAtCenter(textbox, {}, doc.defaultView);
-  yield onInputFocus;
-
+function* testNoAutoFocus(doc) {
+  yield focusNode(doc, "#box4-input");
   is(getFocusedDocument(doc), doc, "Focus is in the XUL document");
 
-  let tooltip = new HTMLTooltip({doc}, {autofocus: true});
-  let tooltipNode = getTooltipContent(doc);
-  yield tooltip.setContent(tooltipNode, 150, 50);
+  info("Test a tooltip without autofocus will not take focus");
+  let tooltip = yield createTooltip(doc, false);
 
   yield showTooltip(tooltip, doc.getElementById("box1"));
-  is(getFocusedDocument(doc), tooltipNode.ownerDocument,
+  is(getFocusedDocument(doc), doc, "Focus is still in the XUL document");
+  ok(doc.activeElement.closest("#box4-input"), "Focus is in the #box4-input");
+
+  yield hideTooltip(tooltip);
+  yield blurNode(doc, "#box4-input");
+}
+
+function* testAutoFocus(doc) {
+  yield focusNode(doc, "#box4-input");
+  is(getFocusedDocument(doc), doc, "Focus is in the XUL document");
+
+  info("Test autofocus tooltip takes focus when displayed, " +
+    "and restores the focus when hidden");
+  let tooltip = yield createTooltip(doc, true);
+
+  yield showTooltip(tooltip, doc.getElementById("box1"));
+  is(getFocusedDocument(doc), tooltip.panel.ownerDocument,
     "Focus is in the tooltip document");
 
   yield hideTooltip(tooltip);
+  is(getFocusedDocument(doc), doc, "Focus is back in the XUL document");
+  ok(doc.activeElement.closest("#box4-input"), "Focus is in the #box4-input");
+
+  info("Blur the textbox before moving to the next test to reset the state.");
+  yield blurNode(doc, "#box4-input");
 }
 
-function* testTooltipWithoutAutoFocus(doc) {
-  info("Test a tooltip can be closed by clicking outside");
-  let textbox = doc.querySelector("textbox");
-
-  info("Focus a XUL textbox");
-  let onInputFocus = once(textbox, "focus");
-  EventUtils.synthesizeMouseAtCenter(textbox, {}, doc.defaultView);
-  yield onInputFocus;
-
+function* testAutoFocusPreservesFocusChange(doc) {
+  yield focusNode(doc, "#box4-input");
   is(getFocusedDocument(doc), doc, "Focus is in the XUL document");
 
-  let tooltip = new HTMLTooltip({doc}, {autofocus: false});
-  let tooltipNode = getTooltipContent(doc);
-  yield tooltip.setContent(tooltipNode, 150, 50);
+  info("Test autofocus tooltip takes focus when displayed, " +
+    "but does not try to restore the active element if it is not focused when hidden");
+  let tooltip = yield createTooltip(doc, true);
 
   yield showTooltip(tooltip, doc.getElementById("box1"));
+  is(getFocusedDocument(doc), tooltip.panel.ownerDocument,
+    "Focus is in the tooltip document");
+
+  info("Move the focus to #box3-input while the tooltip is displayed");
+  yield focusNode(doc, "#box3-input");
+  is(getFocusedDocument(doc), doc, "Focus is back in the XUL document");
+  ok(doc.activeElement.closest("#box3-input"), "Focus is in the #box3-input");
+
+  yield hideTooltip(tooltip);
   is(getFocusedDocument(doc), doc, "Focus is still in the XUL document");
 
-  yield hideTooltip(tooltip);
+  ok(doc.activeElement.closest("#box3-input"), "Focus is still in the #box3-input");
+
+  info("Blur the textbox before moving to the next test to reset the state.");
+  yield blurNode(doc, "#box3-input");
 }
 
 function getFocusedDocument(doc) {
   let activeElement = doc.activeElement;
   while (activeElement && activeElement.contentDocument) {
     activeElement = activeElement.contentDocument.activeElement;
   }
   return activeElement.ownerDocument;
 }
 
-function getTooltipContent(doc) {
+/**
+ * Fpcus the node corresponding to the provided selector in the provided document. Returns
+ * a promise that will resolve when receiving the focus event on the node.
+ */
+function focusNode(doc, selector) {
+  let node = doc.querySelector(selector);
+  let onFocus = once(node, "focus");
+  node.focus();
+  return onFocus;
+}
+
+/**
+ * Blur the node corresponding to the provided selector in the provided document. Returns
+ * a promise that will resolve when receiving the blur event on the node.
+ */
+function blurNode(doc, selector) {
+  let node = doc.querySelector(selector);
+  let onBlur = once(node, "blur");
+  node.blur();
+  return onBlur;
+}
+
+/**
+ * Create an HTMLTooltip instance with the provided autofocus setting.
+ *
+ * @param {Document} doc
+ *        Document in which the tooltip should be created
+ * @param {Boolean} autofocus
+ * @return {Promise} promise that will resolve the HTMLTooltip instance created when the
+ *         tooltip content will be ready.
+ */
+function* createTooltip(doc, autofocus) {
+  let tooltip = new HTMLTooltip({doc}, {autofocus});
   let div = doc.createElementNS(HTML_NS, "div");
   div.style.height = "50px";
-  div.style.boxSizing = "border-box";
-  return div;
+  yield tooltip.setContent(div, 150, 50);
+  return tooltip;
 }

--- a/devtools/client/shared/widgets/HTMLTooltip.js
+++ b/devtools/client/shared/widgets/HTMLTooltip.js
@@ -186,16 +186,17 @@ HTMLTooltip.prototype = {
 
       if (this.type === TYPE.ARROW) {
         this.arrow.style.left = computedPosition.arrowLeft + "px";
       }
 
       this.container.classList.add("tooltip-visible");
 
       this.attachEventsTimer = this.doc.defaultView.setTimeout(() => {
+        this._focusedElement = this.doc.activeElement;
         if (this.autofocus) {
           this.frame.focus();
         }
         this.topWindow.addEventListener("click", this._onClick, true);
         this.emit("shown");
       }, 0);
     });
   },
@@ -206,16 +207,21 @@ HTMLTooltip.prototype = {
    */
   hide: function () {
     this.doc.defaultView.clearTimeout(this.attachEventsTimer);
 
     if (this.isVisible()) {
       this.topWindow.removeEventListener("click", this._onClick, true);
       this.container.classList.remove("tooltip-visible");
       this.emit("hidden");
+
+      if (this.container.contains(this.doc.activeElement) && this._focusedElement) {
+        this._focusedElement.focus();
+        this._focusedElement = null;
+      }
     }
   },
 
   /**
    * Check if the tooltip is currently displayed.
    * @return {Boolean} true if the tooltip is visible
    */
   isVisible: function () {