diff --git a/src/vs/base/browser/ui/hover/hover.css b/src/vs/base/browser/ui/hover/hover.css
index 5cd824a3d76..f3058d6c107 100644
--- a/src/vs/base/browser/ui/hover/hover.css
+++ b/src/vs/base/browser/ui/hover/hover.css
@@ -114,6 +114,11 @@
 	line-height: 22px;
 }
 
+.monaco-hover .hover-row.status-bar .info {
+	font-style: italic;
+	padding: 0px 8px;
+}
+
 .monaco-hover .hover-row.status-bar .actions {
 	display: flex;
 	padding: 0px 8px;
diff --git a/src/vs/workbench/services/hover/browser/hover.ts b/src/vs/workbench/services/hover/browser/hover.ts
index 1f1de94425a..1c850be8540 100644
--- a/src/vs/workbench/services/hover/browser/hover.ts
+++ b/src/vs/workbench/services/hover/browser/hover.ts
@@ -93,6 +93,14 @@ export interface IHoverOptions {
 	 */
 	hideOnHover?: boolean;
 
+	/**
+	 * When {@link hideOnHover} is explicitly true or undefined and its auto value is detected to
+	 * hide, show a hint at the bottom of the hover explaining how to mouse over the widget. This
+	 * should be used in the cases where despite the hover having no interactive content, it's
+	 * likely the user may want to interact with it somehow.
+	 */
+	showHoverHint?: boolean;
+
 	/**
 	 * Whether to hide the hover when a key is pressed.
 	 */
diff --git a/src/vs/workbench/services/hover/browser/hoverWidget.ts b/src/vs/workbench/services/hover/browser/hoverWidget.ts
index b227a4ac141..0dc0d9f4830 100644
--- a/src/vs/workbench/services/hover/browser/hoverWidget.ts
+++ b/src/vs/workbench/services/hover/browser/hoverWidget.ts
@@ -18,6 +18,8 @@ import { IOpenerService } from 'vs/platform/opener/common/opener';
 import { IInstantiationService } from 'vs/platform/instantiation/common/instantiation';
 import { MarkdownRenderer, openLinkFromMarkdown } from 'vs/editor/contrib/markdownRenderer/browser/markdownRenderer';
 import { isMarkdownString } from 'vs/base/common/htmlContent';
+import { localize } from 'vs/nls';
+import { isMacintosh } from 'vs/base/common/platform';
 
 const $ = dom.$;
 type TargetRect = {
@@ -191,19 +193,31 @@ export class HoverWidget extends Widget {
 		}
 		this._hoverContainer.appendChild(this._hover.containerDomNode);
 
+		// Determine whether to hide on hover
 		let hideOnHover: boolean;
 		if (options.actions && options.actions.length > 0) {
 			// If there are actions, require hover so they can be accessed
 			hideOnHover = false;
 		} else {
 			if (options.hideOnHover === undefined) {
-				// Defaults to true when string, false when markdown as it may contain links
-				hideOnHover = typeof options.content === 'string';
+				// When unset, will default to true when it's a string or when it's markdown that
+				// appears to have a link using a naive check for ']('
+				hideOnHover = typeof options.content === 'string' || isMarkdownString(options.content) && !options.content.value.includes('](');
 			} else {
 				// It's set explicitly
 				hideOnHover = options.hideOnHover;
 			}
 		}
+
+		// Show the hover hint if needed
+		if (hideOnHover && options.showHoverHint) {
+			const statusBarElement = $('div.hover-row.status-bar');
+			const infoElement = $('div.info');
+			infoElement.textContent = localize('hoverhint', 'Hold {0} key to mouse over', isMacintosh ? 'Option' : 'Alt');
+			statusBarElement.appendChild(infoElement);
+			this._hover.containerDomNode.appendChild(statusBarElement);
+		}
+
 		const mouseTrackerTargets = [...this._target.targetElements];
 		if (!hideOnHover) {
 			mouseTrackerTargets.push(this._hoverContainer);
@@ -453,14 +467,36 @@ export class HoverWidget extends Widget {
 
 		// Position hover on right to target
 		if (this._hoverPosition === HoverPosition.RIGHT) {
+			const roomOnRight = document.documentElement.clientWidth - target.right;
 			// Hover on the right is going beyond window.
-			if (target.right + this._hover.containerDomNode.clientWidth >= document.documentElement.clientWidth) {
-				this._hoverPosition = HoverPosition.LEFT;
+			if (roomOnRight < this._hover.containerDomNode.clientWidth) {
+				const roomOnLeft = target.left;
+				// There's enough room on the left, flip the hover position
+				if (roomOnLeft >= this._hover.containerDomNode.clientWidth) {
+					this._hoverPosition = HoverPosition.LEFT;
+				}
+				// Hover on the left would go beyond window too
+				else {
+					this._hoverPosition = HoverPosition.BELOW;
+				}
 			}
 		}
-
 		// Position hover on left to target
-		if (this._hoverPosition === HoverPosition.LEFT) {
+		else if (this._hoverPosition === HoverPosition.LEFT) {
+
+			const roomOnLeft = target.left;
+			// Hover on the left is going beyond window.
+			if (roomOnLeft < this._hover.containerDomNode.clientWidth) {
+				const roomOnRight = document.documentElement.clientWidth - target.right;
+				// There's enough room on the right, flip the hover position
+				if (roomOnRight >= this._hover.containerDomNode.clientWidth) {
+					this._hoverPosition = HoverPosition.RIGHT;
+				}
+				// Hover on the right would go beyond window too
+				else {
+					this._hoverPosition = HoverPosition.BELOW;
+				}
+			}
 			// Hover on the left is going beyond window.
 			if (target.left - this._hover.containerDomNode.clientWidth <= document.documentElement.clientLeft) {
 				this._hoverPosition = HoverPosition.RIGHT;
diff --git a/src/vs/workbench/services/quickinput/browser/quickInputService.ts b/src/vs/workbench/services/quickinput/browser/quickInputService.ts
index 77498318db2..4e511787aa4 100644
--- a/src/vs/workbench/services/quickinput/browser/quickInputService.ts
+++ b/src/vs/workbench/services/quickinput/browser/quickInputService.ts
@@ -72,7 +72,7 @@ class QuickInputHoverDelegate implements IHoverDelegate {
 	showHover(options: IHoverDelegateOptions, focus?: boolean): IHoverWidget | undefined {
 		return this.hoverService.showHover({
 			...options,
-			hideOnHover: false,
+			showHoverHint: true,
 			hideOnKeyDown: false,
 			skipFadeInAnimation: true,
 		}, focus);