--- a/devtools/client/preferences/devtools-client.js
+++ b/devtools/client/preferences/devtools-client.js
@@ -283,18 +283,22 @@ pref("devtools.netmonitor.persistlog", f
 // in the Web Console to display a timestamp, or |false| to not display
 // any timestamps.
 pref("devtools.webconsole.timestampMessages", false);
 
 // Web Console automatic multiline mode: |true| if you want incomplete statements
 // 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);
 
 // Enable client-side mapping service for source maps
 pref("devtools.source-map.client-service.enabled", true);
 
 // The number of lines that are displayed in the web console.

--- a/devtools/client/webconsole/test/mochitest/browser_console_context_menu_entries.js
+++ b/devtools/client/webconsole/test/mochitest/browser_console_context_menu_entries.js
@@ -27,17 +27,18 @@ add_task(async function() {
   ok(menuPopup, "The context menu is displayed on a network message");
 
   let expectedContextMenu = [
     "#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)",
+    "#console-menu-open-sidebar (V) [disabled]",
   ];
   is(getSimplifiedContextMenu(menuPopup).join("\n"), expectedContextMenu.join("\n"),
     "The context menu has the expected entries for a network message");
 
   info("Logging a text message in the content window");
   const onLogMessage = waitForMessage(hud, "simple text message");
   ContentTask.spawn(gBrowser.selectedBrowser, null, () => {
     content.wrappedJSObject.console.log("simple text message");
@@ -46,17 +47,18 @@ add_task(async function() {
   const logMessage = await onLogMessage;
   menuPopup = await openContextMenu(hud, logMessage.node);
   ok(menuPopup, "The context menu is displayed on a log message");
 
   expectedContextMenu = [
     "#console-menu-store (S) [disabled]",
     "#console-menu-copy (C)",
     "#console-menu-copy-object (o) [disabled]",
-    "#console-menu-select (A)"
+    "#console-menu-select (A)",
+    "#console-menu-open-sidebar (V) [disabled]",
   ];
   is(getSimplifiedContextMenu(menuPopup).join("\n"), expectedContextMenu.join("\n"),
     "The context menu has the expected entries for a simple log message");
 
   await hideContextMenu(hud);
 });
 
 function getSimplifiedContextMenu(popupElement) {