--- a/devtools/client/webconsole/components/JSTerm.js
+++ b/devtools/client/webconsole/components/JSTerm.js
@@ -304,25 +304,16 @@ class JSTerm extends Component {
               ) {
                 return null;
               }
 
               this.clearCompletion();
               return "CodeMirror.Pass";
             },
 
-            "Esc": () => {
-              if (this.autocompletePopup.isOpen) {
-                this.clearCompletion();
-                return null;
-              }
-
-              return "CodeMirror.Pass";
-            },
-
             "PageUp": () => {
               if (this.autocompletePopup.isOpen) {
                 this.complete(this.COMPLETE_PAGEUP);
                 return null;
               }
 
               return "CodeMirror.Pass";
             },
@@ -348,25 +339,35 @@ class JSTerm extends Component {
             "End": () => {
               if (this.autocompletePopup.isOpen) {
                 this.autocompletePopup.selectedIndex =
                   this.autocompletePopup.itemCount - 1;
                 return null;
               }
 
               return "CodeMirror.Pass";
-            }
+            },
+
+            "Esc": false,
           }
         });
 
         this.editor.on("change", this._inputEventHandler);
         this.editor.appendToLocalElement(this.node);
         const cm = this.editor.codeMirror;
         cm.on("paste", (_, event) => this.props.onPaste(event));
         cm.on("drop", (_, event) => this.props.onPaste(event));
+
+        this.node.addEventListener("keydown", event => {
+          if (event.keyCode === KeyCodes.DOM_VK_ESCAPE && this.autocompletePopup.isOpen) {
+            this.clearCompletion();
+            event.preventDefault();
+            event.stopPropagation();
+          }
+        });
       }
     } else if (this.inputNode) {
       this.inputNode.addEventListener("keypress", this._keyPress);
       this.inputNode.addEventListener("input", this._inputEventHandler);
       this.inputNode.addEventListener("keyup", this._inputEventHandler);
       this.focus();
     }
 

--- a/devtools/client/webconsole/test/mochitest/browser_webconsole_split.js
+++ b/devtools/client/webconsole/test/mochitest/browser_webconsole_split.js
@@ -7,21 +7,30 @@
 
 const TEST_URI = "data:text/html;charset=utf-8,Web Console test for splitting";
 const {Toolbox} = require("devtools/client/framework/toolbox");
 const {LocalizationHelper} = require("devtools/shared/l10n");
 const L10N =
   new LocalizationHelper("devtools/client/locales/toolbox.properties");
 
 // Test is slow on Linux EC2 instances - Bug 962931
-requestLongerTimeout(2);
+requestLongerTimeout(4);
 
 add_task(async function() {
+  // Run test with legacy JsTerm
+  await pushPref("devtools.webconsole.jsterm.codeMirror", false);
+  await performTests();
+  // And then run it with the CodeMirror-powered one.
+  await pushPref("devtools.webconsole.jsterm.codeMirror", true);
+  await performTests();
+});
+
+async function performTests() {
   let toolbox;
-
+  await pushPref("devtools.webconsole.jsterm.codeMirror", true);
   await addTab(TEST_URI);
   await testConsoleLoadOnDifferentPanel();
   await testKeyboardShortcuts();
   await checkAllTools();
 
   info("Testing host types");
   checkHostType(Toolbox.HostType.BOTTOM);
   await checkToolboxUI();
@@ -244,9 +253,9 @@ add_task(async function() {
   }
 
   function checkHostType(hostType) {
     is(toolbox.hostType, hostType, "host type is " + hostType);
 
     const pref = Services.prefs.getCharPref("devtools.toolbox.host");
     is(pref, hostType, "host pref is " + hostType);
   }
-});
+}