diff --git a/packages/core/src/components/hotkeys/hotkeysDialog.tsx b/packages/core/src/components/hotkeys/hotkeysDialog.tsx
index c2632595344..e48d3e974e3 100644
--- a/packages/core/src/components/hotkeys/hotkeysDialog.tsx
+++ b/packages/core/src/components/hotkeys/hotkeysDialog.tsx
@@ -22,6 +22,12 @@ export interface IHotkeysDialogProps extends IDialogProps {
     globalHotkeysGroup?: string;
 }
 
+/**
+ * The delay before showing or hiding the dialog. Should be long enough to
+ * allow all registered hotkey listeners to execute first.
+ */
+const DELAY_IN_MS = 10;
+
 class HotkeysDialog {
     public componentProps = {
         globalHotkeysGroup: "Global hotkeys",
@@ -30,7 +36,8 @@ class HotkeysDialog {
     private container: HTMLElement;
     private hotkeysQueue = [] as IHotkeyProps[][];
     private isDialogShowing = false;
-    private timeoutToken = 0;
+    private showTimeoutToken: number;
+    private hideTimeoutToken: number;
 
     public render() {
         if (this.container == null) {
@@ -59,8 +66,13 @@ class HotkeysDialog {
         this.hotkeysQueue.push(hotkeys);
 
         // reset timeout for debounce
-        clearTimeout(this.timeoutToken);
-        this.timeoutToken = setTimeout(this.show, 10);
+        clearTimeout(this.showTimeoutToken);
+        this.showTimeoutToken = setTimeout(this.show, DELAY_IN_MS);
+    }
+
+    public hideAfterDelay() {
+        clearTimeout(this.hideTimeoutToken);
+        this.hideTimeoutToken = setTimeout(this.hide, DELAY_IN_MS);
     }
 
     public show = () => {
@@ -141,3 +153,12 @@ export function showHotkeysDialog(hotkeys: IHotkeyProps[]) {
 export function hideHotkeysDialog() {
     HOTKEYS_DIALOG.hide();
 }
+
+/**
+ * Use this function instead of `hideHotkeysDialog` if you need to ensure that all hotkey listeners
+ * have time to execute with the dialog in a consistent open state. This can avoid flickering the
+ * dialog between open and closed states as successive listeners fire.
+ */
+export function hideHotkeysDialogAfterDelay() {
+    HOTKEYS_DIALOG.hideAfterDelay();
+}
diff --git a/packages/core/src/components/hotkeys/hotkeysEvents.ts b/packages/core/src/components/hotkeys/hotkeysEvents.ts
index a947a45ffb5..d848d122a47 100644
--- a/packages/core/src/components/hotkeys/hotkeysEvents.ts
+++ b/packages/core/src/components/hotkeys/hotkeysEvents.ts
@@ -11,7 +11,7 @@ import { safeInvoke } from "../../common/utils";
 import { Hotkey, IHotkeyProps } from "./hotkey";
 import { comboMatches, getKeyCombo, IKeyCombo, parseKeyCombo } from "./hotkeyParser";
 import { IHotkeysProps } from "./hotkeys";
-import { isHotkeysDialogShowing, showHotkeysDialog } from "./hotkeysDialog";
+import { hideHotkeysDialogAfterDelay, isHotkeysDialogShowing, showHotkeysDialog } from "./hotkeysDialog";
 
 const SHOW_DIALOG_KEY = "?";
 
@@ -53,15 +53,17 @@ export class HotkeysEvents {
     }
 
     public handleKeyDown = (e: KeyboardEvent) => {
-        if (isHotkeysDialogShowing()) {
-            return;
-        }
-
         const combo = getKeyCombo(e);
         const isTextInput = this.isTextInput(e);
 
         if (!isTextInput && comboMatches(parseKeyCombo(SHOW_DIALOG_KEY), combo)) {
-            showHotkeysDialog(this.actions.map((action) => action.props));
+            if (isHotkeysDialogShowing()) {
+                hideHotkeysDialogAfterDelay();
+            } else {
+                showHotkeysDialog(this.actions.map((action) => action.props));
+            }
+            return;
+        } else if (isHotkeysDialogShowing()) {
             return;
         }