--- a/browser/themes/shared/devtools/dark-theme.css
+++ b/browser/themes/shared/devtools/dark-theme.css
@@ -379,25 +379,16 @@ div.CodeMirror span.eval-text {
   color: white;
   border-bottom: 1px solid #434850;
 }
 
 .theme-tooltip-panel .devtools-tooltip-simple-text:last-child {
   border-bottom: 0;
 }
 
-.devtools-horizontal-splitter {
-  border-bottom: 1px solid var(--theme-splitter-color);
-}
-
-.devtools-side-splitter {
-  -moz-border-end: 1px solid var(--theme-splitter-color);
-  border-color: var(--theme-splitter-color); /* Needed for responsive container at low width. */
-}
-
 .devtools-textinput,
 .devtools-searchinput {
   background-color: rgba(24, 29, 32, 1);
   color: rgba(184, 200, 217, 1);
 }
 
 .CodeMirror-Tern-fname {
   color: #f7f7f7;

--- a/browser/themes/shared/devtools/light-theme.css
+++ b/browser/themes/shared/devtools/light-theme.css
@@ -388,25 +388,16 @@ div.CodeMirror span.eval-text {
   color: black;
   border-bottom: 1px solid #d9e1e8;
 }
 
 .theme-tooltip-panel .devtools-tooltip-simple-text:last-child {
   border-bottom: 0;
 }
 
-.devtools-horizontal-splitter {
-  border-bottom: 1px solid var(--theme-splitter-color);
-}
-
-.devtools-side-splitter {
-  -moz-border-end: 1px solid var(--theme-splitter-color);
-  border-color: var(--theme-splitter-color); /* Needed for responsive container at low width. */
-}
-
 .CodeMirror-hints,
 .CodeMirror-Tern-tooltip {
   box-shadow: 0 0 4px rgba(128, 128, 128, .5);
   background-color: var(--theme-sidebar-background);
 }
 
 
 %include toolbars.inc.css

--- a/browser/themes/shared/devtools/toolbars.inc.css
+++ b/browser/themes/shared/devtools/toolbars.inc.css
@@ -848,8 +848,18 @@
 .hidden-labels-box:not(.visible) > label,
 .hidden-labels-box.visible ~ .hidden-labels-box > label:last-child {
   display: none;
 }
 
 .devtools-invisible-splitter {
   border-color: transparent;
 }
+
+.devtools-horizontal-splitter {
+  border-bottom: 1px solid var(--theme-splitter-color);
+}
+
+.devtools-side-splitter {
+  -moz-border-end: 1px solid var(--theme-splitter-color);
+  border-color: var(--theme-splitter-color); /* Needed for responsive container at low width. */
+}
+

--- a/browser/themes/shared/devtools/widgets.inc.css
+++ b/browser/themes/shared/devtools/widgets.inc.css
@@ -45,23 +45,30 @@
 }
 
 @media (max-width: 700px) {
   .devtools-responsive-container {
     -moz-box-orient: vertical;
   }
 
   .devtools-responsive-container > .devtools-side-splitter {
-    border-width: 0;
-    border-top-width: 1px;
-    border-top-style: solid;
-    margin: 0;
+    /* This is a normally vertical splitter, but we have turned it horizontal
+       due to the smaller resolution */
     min-height: 3px;
     height: 3px;
-    margin-bottom: -3px;
+    margin-top: -3px;
+
+    /* Reset the vertical splitter styles */
+    border-width: 0;
+    border-bottom-width: 1px;
+    border-bottom-style: solid;
+    -moz-margin-start: 0;
+    width: auto;
+    min-width: 0;
+
     /* In some edge case the cursor is not changed to n-resize */
     cursor: n-resize;
   }
 
   .devtools-responsive-container > .devtools-sidebar-tabs {
     min-height: 35vh;
     max-height: 75vh;
   }