diff --git a/components/page/demo/page-component.js b/components/page/demo/page-component.js
index 19527902733..a5a628093d8 100644
--- a/components/page/demo/page-component.js
+++ b/components/page/demo/page-component.js
@@ -27,13 +27,13 @@ import '../../selection/selection-action.js';
 import '../../switch/switch-visibility.js';
 import '../../switch/switch.js';
 import '../../table/table-controls.js';
-import '../page.js';
 import '../page-footer.js';
 import '../page-main.js';
 import '../page-side-nav.js';
 import '../page-supporting.js';
 import './page-header-full.js';
 import { css, html, LitElement, nothing } from 'lit';
+import { _forceLegacyBrowserMode } from '../page.js';
 import { ifDefined } from 'lit/directives/if-defined.js';
 import { inputLabelStyles } from '../../inputs/input-label-styles.js';
 import { pageHeaderImmersiveActionsDemo } from '../test/page-header-immersive-fixtures.js';
@@ -52,6 +52,7 @@ class PageDemo extends LitElement {
 		header: { type: String, attribute: 'header' },
 		immersiveHeaderTitleType: { type: String, attribute: 'immersive-header-title-type' },
 		layout: { type: String, attribute: 'layout' },
+		legacyBrowserMode: { type: String, attribute: 'legacy-browser-mode' },
 		widthType: { type: String, attribute: 'width-type' },
 		_mainDialogOpened: { state: true },
 		_mainToastOpened: { state: true },
@@ -86,6 +87,8 @@ class PageDemo extends LitElement {
 		this.header = urlParams.get('header') || 'full';
 		this.immersiveHeaderTitleType = urlParams.get('immersiveHeaderTitleType') || 'title-subtitle';
 		this.layout = urlParams.get('layout') || 'main-only';
+		this.legacyBrowserMode = urlParams.has('legacyBrowserMode');
+		if (this.legacyBrowserMode) _forceLegacyBrowserMode(true);
 		this.widthType = urlParams.get('widthType') || 'normal';
 		this._mainDialogOpened = false;
 		this._mainToastOpened = false;
@@ -124,6 +127,13 @@ class PageDemo extends LitElement {
 		this.#updateUrlParam('layout', this.layout);
 	}
 
+	#handleLegacyBrowserModeChange(e) {
+		this.legacyBrowserMode = e.target.on;
+		_forceLegacyBrowserMode(this.legacyBrowserMode);
+		this.#updateUrlParamBool('legacyBrowserMode', this.legacyBrowserMode);
+		this.shadowRoot.querySelector('d2l-page')?.requestUpdate();
+	}
+
 	#handleMainDialogClose() {
 		this._mainDialogOpened = false;
 		this._mainToastOpened = true;
@@ -251,6 +261,9 @@ class PageDemo extends LitElement {
 								${this.layout === 'side-nav' ? html`<d2l-switch text="Side Nav" data-key="hasSideNavHeader" @change="${this.#handleVisibilityChange}" ?on="${this.hasSideNavHeader}"></d2l-switch>` : nothing}
 								${this.layout === 'supporting' ? html`<d2l-switch text="Supporting" data-key="hasSupportingHeader" @change="${this.#handleVisibilityChange}" ?on="${this.hasSupportingHeader}"></d2l-switch>` : nothing}
 							</d2l-input-fieldset>
+							<d2l-input-fieldset label="Legacy Browser Mode">
+								<d2l-switch text="On" @change="${this.#handleLegacyBrowserModeChange}" ?on="${this.legacyBrowserMode}"></d2l-switch>
+							</d2l-input-fieldset>
 						</div>
 					</d2l-input-fieldset>
 					${this.#renderDemoHeaderControls()}
diff --git a/components/page/page-main.js b/components/page/page-main.js
index ad82de676ea..614a5fcf535 100644
--- a/components/page/page-main.js
+++ b/components/page/page-main.js
@@ -11,7 +11,7 @@ class PageMain extends PagePanelMixin(LitElement) {
 
 	static styles = [pagePanelStyles, css`
 		.panel-header {
-			top: var(--d2l-page-header-height, 0);
+			top: var(--d2l-page-main-sticky-top, 0);
 		}
 	`];
 
diff --git a/components/page/page.js b/components/page/page.js
index 6791db83bb1..4b9d13708c2 100644
--- a/components/page/page.js
+++ b/components/page/page.js
@@ -11,6 +11,22 @@ const DRAWER_MIN_HEIGHT = 200; // TO DO: Confirm
 const MAIN_MIN_WIDTH = 600; // TO DO: Confirm
 const PANEL_MIN_WIDTH = 320;
 
+/*
+* Legacy Browser Mode can be deleted once we have hard-blocked all browsers that do not support the Popover api,
+* and dialog will be able to escape stacking contexts. It creates a "scrolling container" layout for pages with panels,
+* to avoid the stacking context created by position: sticky.
+*/
+let forceLegacyBrowserMode = false;
+const isPopoverSupported = ('popover' in HTMLElement.prototype);
+function isLegacyBrowserMode() {
+	return forceLegacyBrowserMode || !isPopoverSupported;
+}
+// Back door for the demo page and unit tests to force legacy browser mode, bypassing popover feature detection.
+// DO NOT use in production.
+export function _forceLegacyBrowserMode(on) {
+	forceLegacyBrowserMode = on;
+}
+
 class PanelStateController {
 	constructor(host, panelConfigs) {
 		this.#host = host;
@@ -117,11 +133,12 @@ class Page extends ProviderMixin(LocalizeCoreElement(LitElement)) {
 			max-width: var(--d2l-page-content-max-width, 100%);
 			padding-bottom: var(--d2l-page-footer-height, 0); /* Reserve space for fixed footer */
 		}
-		.content.has-panels {
+		.page.has-panels .content {
 			min-height: calc(100vh - var(--d2l-page-header-height-measured, 0px));
 		}
 
 		main {
+			--d2l-page-main-sticky-top: var(--d2l-page-header-height, 0);
 			flex: 1;
 			min-width: min(${MAIN_MIN_WIDTH}px, 100%);
 		}
@@ -160,6 +177,43 @@ class Page extends ProviderMixin(LocalizeCoreElement(LitElement)) {
 			margin-inline: var(--d2l-page-margin-inline, 0);
 			max-width: var(--d2l-page-footer-max-width, 100%);
 		}
+
+		/* Legacy Browser Mode */
+		.page.legacy-browser-mode.has-panels {
+			display: flex;
+			flex-direction: column;
+			height: 100vh;
+		}
+		.page.legacy-browser-mode.has-panels .header,
+		.page.legacy-browser-mode.header-sticky.has-panels .header {
+			flex: 0 0 auto;
+			position: static;
+		}
+		.page.legacy-browser-mode.has-panels .content {
+			flex: 1 1 auto;
+			min-height: 0;
+			overflow: hidden;
+			padding-bottom: 0;
+			width: 100%;
+		}
+		.page.legacy-browser-mode.has-panels main {
+			--d2l-page-main-sticky-top: 0; /* Header is static and content scrolls within main, so panel headers stick to the top of the scroll container */
+			min-height: 0;
+			overflow: auto;
+		}
+		.page.legacy-browser-mode.has-panels .side-nav-panel,
+		.page.legacy-browser-mode.has-panels .supporting-panel,
+		.page.legacy-browser-mode.has-panels .divider {
+			max-height: none;
+			min-height: 0;
+			position: static;
+		}
+		.page.legacy-browser-mode.has-panels .footer {
+			flex: 0 0 auto;
+		}
+		.page.legacy-browser-mode.has-panels .fixed-footer {
+			position: static;
+		}
 	`;
 
 	constructor() {
@@ -229,17 +283,15 @@ class Page extends ProviderMixin(LocalizeCoreElement(LitElement)) {
 	render() {
 		const pageClasses = {
 			'page': true,
-			'header-sticky': this._headerIsSticky
-		};
-		const contentClasses = {
-			'content': true,
+			'header-sticky': this._headerIsSticky,
+			'legacy-browser-mode': isLegacyBrowserMode(),
 			'has-panels': this._slotVisibility['side-nav'] || this._slotVisibility['supporting']
 		};
 
 		return html`
 			<div class="${classMap(pageClasses)}">
 				${this.#renderHeader()}
-				<div class="${classMap(contentClasses)}">
+				<div class="content">
 					${this.#renderSideNavPanel()}
 					<main><slot></slot></main>
 					${this.#renderSupportingPanel()}