--- a/devtools/client/webconsole/components/JSTerm.js
+++ b/devtools/client/webconsole/components/JSTerm.js
@@ -124,24 +124,16 @@ class JSTerm extends Component {
     this._lastFrameActorId = null;
 
     /**
      * Last input value.
      * @type string
      */
     this.lastInputValue = "";
 
-    /**
-     * Tells if the autocomplete popup was navigated since the last open.
-     *
-     * @private
-     * @type boolean
-     */
-    this._autocompletePopupNavigated = false;
-
     this.autocompletePopup = null;
     this.inputNode = null;
     this.completeNode = null;
 
     this.COMPLETE_FORWARD = 0;
     this.COMPLETE_BACKWARD = 1;
     this.COMPLETE_HINT_ONLY = 2;
     this.COMPLETE_PAGEUP = 3;
@@ -187,19 +179,19 @@ class JSTerm extends Component {
               if (
                 !this.autocompletePopup.isOpen &&
                 !Debugger.isCompilableUnit(this.getInputValue())
               ) {
                 // incomplete statement
                 return "CodeMirror.Pass";
               }
 
-              if (this._autocompletePopupNavigated &&
-                this.autocompletePopup.isOpen &&
-                this.autocompletePopup.selectedIndex > -1
+              if (
+                this.autocompletePopup.isOpen
+                && this.autocompletePopup.selectedIndex > -1
               ) {
                 return this.acceptProposedCompletion();
               }
 
               this.execute();
               return null;
             },
 
@@ -226,36 +218,30 @@ class JSTerm extends Component {
               // Input is not empty and some text is selected, let the editor handle this.
               return true;
             },
 
             "Up": () => {
               let inputUpdated;
               if (this.autocompletePopup.isOpen) {
                 inputUpdated = this.complete(this.COMPLETE_BACKWARD);
-                if (inputUpdated) {
-                  this._autocompletePopupNavigated = true;
-                }
               } else if (this.canCaretGoPrevious()) {
                 inputUpdated = this.historyPeruse(HISTORY_BACK);
               }
 
               if (!inputUpdated) {
                 return "CodeMirror.Pass";
               }
               return null;
             },
 
             "Down": () => {
               let inputUpdated;
               if (this.autocompletePopup.isOpen) {
                 inputUpdated = this.complete(this.COMPLETE_FORWARD);
-                if (inputUpdated) {
-                  this._autocompletePopupNavigated = true;
-                }
               } else if (this.canCaretGoNext()) {
                 inputUpdated = this.historyPeruse(HISTORY_FORWARD);
               }
 
               if (!inputUpdated) {
                 return "CodeMirror.Pass";
               }
               return null;
@@ -266,22 +252,19 @@ class JSTerm extends Component {
                 this.clearCompletion();
               }
               return "CodeMirror.Pass";
             },
 
             "Right": () => {
               const haveSuggestion =
                 this.autocompletePopup.isOpen || this.lastCompletion.value;
-              const useCompletion =
-                this.canCaretGoNext() || this._autocompletePopupNavigated;
 
               if (
                 haveSuggestion &&
-                useCompletion &&
                 this.complete(this.COMPLETE_HINT_ONLY) &&
                 this.lastCompletion.value &&
                 this.acceptProposedCompletion()
               ) {
                 return null;
               }
 
               if (this.autocompletePopup.isOpen) {
@@ -329,30 +312,26 @@ class JSTerm extends Component {
                 return null;
               }
 
               return "CodeMirror.Pass";
             },
 
             "PageUp": () => {
               if (this.autocompletePopup.isOpen) {
-                if (this.complete(this.COMPLETE_PAGEUP)) {
-                  this._autocompletePopupNavigated = true;
-                }
+                this.complete(this.COMPLETE_PAGEUP);
                 return null;
               }
 
               return "CodeMirror.Pass";
             },
 
             "PageDown": () => {
               if (this.autocompletePopup.isOpen) {
-                if (this.complete(this.COMPLETE_PAGEDOWN)) {
-                  this._autocompletePopupNavigated = true;
-                }
+                this.complete(this.COMPLETE_PAGEDOWN);
                 return null;
               }
 
               return "CodeMirror.Pass";
             },
 
             "Home": () => {
               if (this.autocompletePopup.isOpen) {
@@ -840,76 +819,64 @@ class JSTerm extends Component {
         if (this.autocompletePopup.isOpen) {
           this.clearCompletion();
           event.preventDefault();
           event.stopPropagation();
         }
         break;
 
       case KeyCodes.DOM_VK_RETURN:
-        if (this._autocompletePopupNavigated &&
+        if (
             this.autocompletePopup.isOpen &&
             this.autocompletePopup.selectedIndex > -1) {
           this.acceptProposedCompletion();
         } else {
           this.execute();
         }
         event.preventDefault();
         break;
 
       case KeyCodes.DOM_VK_UP:
         if (this.autocompletePopup.isOpen) {
           inputUpdated = this.complete(this.COMPLETE_BACKWARD);
-          if (inputUpdated) {
-            this._autocompletePopupNavigated = true;
-          }
         } else if (this.canCaretGoPrevious()) {
           inputUpdated = this.historyPeruse(HISTORY_BACK);
         }
         if (inputUpdated) {
           event.preventDefault();
         }
         break;
 
       case KeyCodes.DOM_VK_DOWN:
         if (this.autocompletePopup.isOpen) {
           inputUpdated = this.complete(this.COMPLETE_FORWARD);
-          if (inputUpdated) {
-            this._autocompletePopupNavigated = true;
-          }
         } else if (this.canCaretGoNext()) {
           inputUpdated = this.historyPeruse(HISTORY_FORWARD);
         }
         if (inputUpdated) {
           event.preventDefault();
         }
         break;
 
       case KeyCodes.DOM_VK_PAGE_UP:
         if (this.autocompletePopup.isOpen) {
           inputUpdated = this.complete(this.COMPLETE_PAGEUP);
-          if (inputUpdated) {
-            this._autocompletePopupNavigated = true;
-          }
         } else {
           this.hud.outputScroller.scrollTop =
             Math.max(0,
               this.hud.outputScroller.scrollTop -
               this.hud.outputScroller.clientHeight
             );
         }
         event.preventDefault();
         break;
 
       case KeyCodes.DOM_VK_PAGE_DOWN:
         if (this.autocompletePopup.isOpen) {
           inputUpdated = this.complete(this.COMPLETE_PAGEDOWN);
-          if (inputUpdated) {
-            this._autocompletePopupNavigated = true;
-          }
         } else {
           this.hud.outputScroller.scrollTop =
             Math.min(this.hud.outputScroller.scrollHeight,
               this.hud.outputScroller.scrollTop +
               this.hud.outputScroller.clientHeight
             );
         }
         event.preventDefault();
@@ -939,27 +906,23 @@ class JSTerm extends Component {
 
       case KeyCodes.DOM_VK_LEFT:
         if (this.autocompletePopup.isOpen || this.lastCompletion.value) {
           this.clearCompletion();
         }
         break;
 
       case KeyCodes.DOM_VK_RIGHT:
-        const cursorAtTheEnd = this.inputNode.selectionStart ==
-                             this.inputNode.selectionEnd &&
-                             this.inputNode.selectionStart ==
-                             inputValue.length;
-        const haveSuggestion = this.autocompletePopup.isOpen ||
-                             this.lastCompletion.value;
-        const useCompletion = cursorAtTheEnd || this._autocompletePopupNavigated;
-        if (haveSuggestion && useCompletion &&
-            this.complete(this.COMPLETE_HINT_ONLY) &&
-            this.lastCompletion.value &&
-            this.acceptProposedCompletion()) {
+        const haveSuggestion = this.autocompletePopup.isOpen || this.lastCompletion.value;
+        if (
+          haveSuggestion &&
+          this.complete(this.COMPLETE_HINT_ONLY) &&
+          this.lastCompletion.value &&
+          this.acceptProposedCompletion()
+        ) {
           event.preventDefault();
         }
         if (this.autocompletePopup.isOpen) {
           this.clearCompletion();
         }
         break;
 
       case KeyCodes.DOM_VK_TAB:
@@ -1296,17 +1259,17 @@ class JSTerm extends Component {
     const popup = this.autocompletePopup;
     popup.setItems(items);
 
     const completionType = this.lastCompletion.completionType;
     this.lastCompletion = {
       value: inputValue,
       matchProp: lastPart,
     };
-    if (items.length > 1 && !popup.isOpen) {
+    if (items.length > 0 && !popup.isOpen) {
       let popupAlignElement;
       let xOffset;
       let yOffset;
 
       if (this.editor) {
         popupAlignElement = this.node.querySelector(".CodeMirror-cursor");
         // We need to show the popup at the ".".
         xOffset = -1 * lastPart.length * this._inputCharWidth;
@@ -1316,22 +1279,21 @@ class JSTerm extends Component {
           (inputUntilCursor.lastIndexOf("\n") + 1) -
           lastPart.length;
         xOffset = (offset * this._inputCharWidth) + this._chevronWidth;
         popupAlignElement = this.inputNode;
       }
 
       if (popupAlignElement) {
         popup.openPopup(popupAlignElement, xOffset, yOffset);
-        this._autocompletePopupNavigated = false;
       }
-    } else if (items.length < 2 && popup.isOpen) {
+    } else if (items.length === 0 && popup.isOpen) {
       popup.hidePopup();
-      this._autocompletePopupNavigated = false;
     }
+
     if (items.length == 1) {
       popup.selectedIndex = 0;
     }
 
     this.onAutocompleteSelect();
 
     if (completionType != this.COMPLETE_HINT_ONLY && popup.itemCount == 1) {
       this.acceptProposedCompletion();
@@ -1376,17 +1338,16 @@ class JSTerm extends Component {
         // value again.
         if (this.inputNode) {
           this.inputNode.blur();
         }
         this.autocompletePopup.once("popup-closed", () => {
           this.focus();
         });
         this.autocompletePopup.hidePopup();
-        this._autocompletePopupNavigated = false;
       }
     }
   }
 
   /**
    * Accept the proposed input completion.
    *
    * @return boolean

--- a/devtools/client/webconsole/test/mochitest/browser_jsterm_autocomplete_return_key_no_selection.js
+++ b/devtools/client/webconsole/test/mochitest/browser_jsterm_autocomplete_return_key_no_selection.js
@@ -45,20 +45,23 @@ async function performTests() {
   await onPopUpOpen;
 
   ok(popup.isOpen, "popup is open");
   is(popup.itemCount, 2, "popup.itemCount is correct");
   isnot(popup.selectedIndex, -1, "popup.selectedIndex is correct");
 
   info("press Return and wait for popup to hide");
   const onPopUpClose = popup.once("popup-closed");
-  executeSoon(() => EventUtils.synthesizeKey("KEY_Enter"));
+  EventUtils.synthesizeKey("KEY_Enter");
   await onPopUpClose;
 
   ok(!popup.isOpen, "popup is not open after KEY_Enter");
-  is(jsterm.getInputValue(), "", "inputNode is empty after KEY_Enter");
+  is(jsterm.getInputValue(), "window.testBugA",
+    "input was completed with the first item of the popup");
   ok(!getJsTermCompletionValue(jsterm), "completeNode is empty");
 
+  EventUtils.synthesizeKey("KEY_Enter");
+  is(jsterm.getInputValue(), "", "input is empty after KEY_Enter");
+
   const state = ui.consoleOutput.getStore().getState();
   const entries = getHistoryEntries(state);
-  is(entries[entries.length - 1], "window.testBug",
-     "jsterm history is correct");
+  is(entries[entries.length - 1], "window.testBugA", "jsterm history is correct");
 }

--- a/devtools/client/webconsole/test/mochitest/browser_jsterm_completion.js
+++ b/devtools/client/webconsole/test/mochitest/browser_jsterm_completion.js
@@ -14,21 +14,24 @@ add_task(async function() {
   await performTests();
   // And then run it with the CodeMirror-powered one.
   await pushPref("devtools.webconsole.jsterm.codeMirror", true);
   await performTests();
 });
 
 async function performTests() {
   const {jsterm, ui} = await openNewTabAndConsole(TEST_URI);
+  const {autocompletePopup} = jsterm;
 
   // Test typing 'docu'.
   await jstermSetValueAndComplete(jsterm, "docu");
   is(jsterm.getInputValue(), "docu", "'docu' completion (input.value)");
   checkJsTermCompletionValue(jsterm, "    ment", "'docu' completion (completeNode)");
+  is(autocompletePopup.items.length, 1, "autocomplete popup has 1 item");
+  ok(autocompletePopup.isOpen, "autocomplete popup is open with 1 item");
 
   // Test typing 'docu' and press tab.
   await jstermSetValueAndComplete(jsterm, "docu", undefined, jsterm.COMPLETE_FORWARD);
   is(jsterm.getInputValue(), "document", "'docu' tab completion");
 
   checkJsTermCursor(jsterm, "document".length, "cursor is at the end of 'document'");
   is(getJsTermCompletionValue(jsterm).replace(/ /g, ""), "", "'docu' completed");