diff --git a/toolkit/themes/linux/global/autocomplete.css b/toolkit/themes/linux/global/autocomplete.css
index b9cbb536649..fffa2b1f035 100644
--- a/toolkit/themes/linux/global/autocomplete.css
+++ b/toolkit/themes/linux/global/autocomplete.css
@@ -117,23 +117,26 @@ treechildren.autocomplete-treebody::-moz-tree-cell-text(selected) {
   color: MenuText;
 }
 
+.ac-url-box {
+  /* When setting a vertical margin here, half of that needs to be added
+     .ac-title-box's translateY for when .ac-url-box is hidden (see below). */
+  margin-top: 1px;
+}
+
 .autocomplete-richlistitem[actiontype="keyword"] .ac-url-box,
 .autocomplete-richlistitem[actiontype="searchengine"] .ac-url-box,
 .autocomplete-richlistitem[actiontype="visiturl"] .ac-url-box,
 .autocomplete-richlistitem[type~="autofill"] .ac-url-box {
-  display: none;
+  visibility: hidden;
 }
 
 .autocomplete-richlistitem[actiontype="keyword"] .ac-title-box,
 .autocomplete-richlistitem[actiontype="searchengine"] .ac-title-box,
 .autocomplete-richlistitem[actiontype="visiturl"] .ac-title-box,
 .autocomplete-richlistitem[type~="autofill"] .ac-title-box {
-  margin-top: 12px;
-  margin-bottom: 12px;
-}
-
-.ac-url-box {
-  margin-top: 1px;
+  /* Center the title by moving it down by half of .ac-url-box's height,
+     including vertical margins (if any). */
+  transform: translateY(.5em);
 }
 
 .ac-site-icon {
diff --git a/toolkit/themes/osx/global/autocomplete.css b/toolkit/themes/osx/global/autocomplete.css
index 50815a8dbeb..7d0cce2e4cc 100644
--- a/toolkit/themes/osx/global/autocomplete.css
+++ b/toolkit/themes/osx/global/autocomplete.css
@@ -102,23 +102,26 @@ treechildren.autocomplete-treebody::-moz-tree-cell-text(selected) {
   padding: 5px 2px;
 }
 
+.ac-url-box {
+  /* When setting a vertical margin here, half of that needs to be added
+     .ac-title-box's translateY for when .ac-url-box is hidden (see below). */
+  margin-top: 1px;
+}
+
 .autocomplete-richlistitem[actiontype="keyword"] .ac-url-box,
 .autocomplete-richlistitem[actiontype="searchengine"] .ac-url-box,
 .autocomplete-richlistitem[actiontype="visiturl"] .ac-url-box,
 .autocomplete-richlistitem[type~="autofill"] .ac-url-box {
-  display: none;
+  visibility: hidden;
 }
 
 .autocomplete-richlistitem[actiontype="keyword"] .ac-title-box,
 .autocomplete-richlistitem[actiontype="searchengine"] .ac-title-box,
 .autocomplete-richlistitem[actiontype="visiturl"] .ac-title-box,
 .autocomplete-richlistitem[type~="autofill"] .ac-title-box {
-  margin-top: 12px;
-  margin-bottom: 12px;
-}
-
-.ac-url-box {
-  margin-top: 1px;
+  /* Center the title by moving it down by half of .ac-url-box's height,
+     including vertical margins (if any). */
+  transform: translateY(.5em);
 }
 
 .ac-site-icon {
diff --git a/toolkit/themes/windows/global/autocomplete.css b/toolkit/themes/windows/global/autocomplete.css
index f6e918e8930..9d0aacbd021 100644
--- a/toolkit/themes/windows/global/autocomplete.css
+++ b/toolkit/themes/windows/global/autocomplete.css
@@ -130,27 +130,30 @@ treechildren.autocomplete-treebody::-moz-tree-cell-text(selected) {
 }
 %endif
 
+.ac-title-box {
+  margin-top: 4px;
+}
+
+.ac-url-box {
+  /* When setting a vertical margin here, half of that needs to be added
+     .ac-title-box's translateY for when .ac-url-box is hidden (see below). */
+  margin: 1px 0 4px;
+}
+
 .autocomplete-richlistitem[actiontype="keyword"] .ac-url-box,
 .autocomplete-richlistitem[actiontype="searchengine"] .ac-url-box,
 .autocomplete-richlistitem[actiontype="visiturl"] .ac-url-box,
 .autocomplete-richlistitem[type~="autofill"] .ac-url-box {
-  display: none;
+  visibility: hidden;
 }
 
 .autocomplete-richlistitem[actiontype="keyword"] .ac-title-box,
 .autocomplete-richlistitem[actiontype="searchengine"] .ac-title-box,
 .autocomplete-richlistitem[actiontype="visiturl"] .ac-title-box,
 .autocomplete-richlistitem[type~="autofill"] .ac-title-box {
-  margin-top: 12px;
-  margin-bottom: 12px;
-}
-
-.ac-title-box {
-  margin-top: 4px;
-}
-
-.ac-url-box {
-  margin: 1px 0 4px;
+  /* Center the title by moving it down by half of .ac-url-box's height,
+     including vertical margins (if any). */
+  transform: translateY(calc(.5em + 2px));
 }
 
 .ac-site-icon {