diff --git a/devtools/client/preferences/devtools-client.js b/devtools/client/preferences/devtools-client.js
index f1addb51eb60..660cdb02f139 100644
--- a/devtools/client/preferences/devtools-client.js
+++ b/devtools/client/preferences/devtools-client.js
@@ -292,8 +292,12 @@ pref("devtools.webconsole.timestampMessages", false);
 // to automatically trigger multiline editing (equivalent to shift + enter).
 pref("devtools.webconsole.autoMultiline", true);
 
-// Enable the webconsole sidebar toggle
+// Enable the webconsole sidebar toggle in Nightly builds.
+#if defined(NIGHTLY_BUILD)
+pref("devtools.webconsole.sidebarToggle", true);
+#else
 pref("devtools.webconsole.sidebarToggle", false);
+#endif
 
 // Disable the new performance recording panel by default
 pref("devtools.performance.new-panel-enabled", false);
diff --git a/devtools/client/webconsole/test/mochitest/browser_console_context_menu_entries.js b/devtools/client/webconsole/test/mochitest/browser_console_context_menu_entries.js
index 3672a29ab66f..58c19ba7c30d 100644
--- a/devtools/client/webconsole/test/mochitest/browser_console_context_menu_entries.js
+++ b/devtools/client/webconsole/test/mochitest/browser_console_context_menu_entries.js
@@ -26,14 +26,14 @@ add_task(async function() {
   let menuPopup = await openContextMenu(hud, networkMessage.node);
   ok(menuPopup, "The context menu is displayed on a network message");
 
-  let expectedContextMenu = [
+  let expectedContextMenu = addPrefBasedEntries([
     "#console-menu-copy-url (a)",
     "#console-menu-open-url (T)",
     "#console-menu-store (S) [disabled]",
     "#console-menu-copy (C)",
     "#console-menu-copy-object (o) [disabled]",
-    "#console-menu-select (A)"
-  ];
+    "#console-menu-select (A)",
+  ]);
   is(getSimplifiedContextMenu(menuPopup).join("\n"), expectedContextMenu.join("\n"),
     "The context menu has the expected entries for a network message");
 
@@ -47,18 +47,26 @@ add_task(async function() {
   menuPopup = await openContextMenu(hud, logMessage.node);
   ok(menuPopup, "The context menu is displayed on a log message");
 
-  expectedContextMenu = [
+  expectedContextMenu = addPrefBasedEntries([
     "#console-menu-store (S) [disabled]",
     "#console-menu-copy (C)",
     "#console-menu-copy-object (o) [disabled]",
-    "#console-menu-select (A)"
-  ];
+    "#console-menu-select (A)",
+  ]);
   is(getSimplifiedContextMenu(menuPopup).join("\n"), expectedContextMenu.join("\n"),
     "The context menu has the expected entries for a simple log message");
 
   await hideContextMenu(hud);
 });
 
+function addPrefBasedEntries(expectedEntries) {
+  if (Services.prefs.getBoolPref("devtools.webconsole.sidebarToggle", false)) {
+    expectedEntries.push("#console-menu-open-sidebar (V) [disabled]");
+  }
+
+  return expectedEntries;
+}
+
 function getSimplifiedContextMenu(popupElement) {
   return [...popupElement.querySelectorAll("menuitem")]
     .map(entry => {