diff --git a/browser/components/search/content/search.xml b/browser/components/search/content/search.xml
index cfe35fa6e176..ed2ebdf08874 100644
--- a/browser/components/search/content/search.xml
+++ b/browser/components/search/content/search.xml
@@ -640,6 +640,12 @@
         ]]></body>
       </method>
 
+      <!--
+        This method overrides the autocomplete binding's openPopup (essentially
+        duplicating the logic from the autocomplete popup binding's
+        openAutocompletePopup method), modifying it so that the popup is aligned with
+        the inner textbox, but sized to not extend beyond the search bar border.
+      -->
       <method name="openPopup">
         <body><![CDATA[
           var popup = this.popup;
@@ -662,18 +668,26 @@
 
             document.popupNode = null;
 
+            const isRTL = getComputedStyle(this, "").direction == "rtl";
+
             var outerRect = this.getBoundingClientRect();
             var innerRect = this.inputField.getBoundingClientRect();
-            var width = outerRect.right - innerRect.left;
+            if (isRTL) {
+              var width = innerRect.right - outerRect.left;
+            } else {
+              var width = outerRect.right - innerRect.left;
+            }
             popup.setAttribute("width", width > 100 ? width : 100);
 
+            var yOffset = outerRect.bottom - innerRect.bottom;
+
             // setConsumeRollupEvent() before we call openPopup(), 
             // see bug #404438 for more details
             popup.popupBoxObject.setConsumeRollupEvent(
               this.consumeRollupEvent ? 
                 Ci.nsIPopupBoxObject.ROLLUP_CONSUME : 
                 Ci.nsIPopupBoxObject.ROLLUP_NO_CONSUME);
-            popup.openPopup(null, "", innerRect.left, outerRect.bottom, false, false);
+            popup.openPopup(this.inputField, "after_start", 0, yOffset, false, false);
           }
         ]]></body>
       </method>
