diff --git a/docs/publishers/embedding.rst b/docs/publishers/embedding.rst
index 8b170845445..c37fa040ed5 100644
--- a/docs/publishers/embedding.rst
+++ b/docs/publishers/embedding.rst
@@ -23,7 +23,8 @@ above script tag to the document displayed in the iframe. This will display the
 sidebar in the iframe itself.
 
 Additionally Hypothesis has limited support for enabling annotation of iframed
-content while showing the sidebar in the top-level document. To use this:
+content while showing the sidebar in the top-level document where Hypothesis
+was initially loaded. To use this:
 
 1. Add the above script tag to the top-level document
 
@@ -38,6 +39,8 @@ content while showing the sidebar in the top-level document. To use this:
    ...
    </iframe>
 
-This method *only* works for iframes which are same-origin with the top-level
-document. The client will watch for new iframes being added to the document and
-will automatically enable annotation for them.
+This method *only* works for iframes which are direct children of the top-level
+document and have the same origin.
+
+The client will watch for new iframes being added to the document and will
+automatically enable annotation for them.
diff --git a/src/annotator/cross-frame.js b/src/annotator/cross-frame.js
index bbe15620269..290800b55d9 100644
--- a/src/annotator/cross-frame.js
+++ b/src/annotator/cross-frame.js
@@ -63,12 +63,26 @@ export class CrossFrame {
       frameIdentifiers.delete(frame);
     };
 
-    // Initiate connection to the sidebar.
-    const onDiscoveryCallback = (source, origin, token) =>
-      bridge.createChannel(source, origin, token);
-    discovery.startDiscovery(onDiscoveryCallback);
     frameObserver.observe(injectIntoFrame, iframeUnloaded);
 
+    /**
+     * Attempt to connect to the sidebar frame.
+     *
+     * @param {Window} frame
+     * @return {Promise<void>}
+     */
+    this.connectToSidebar = frame => {
+      return new Promise(resolve => {
+        discovery.startDiscovery(
+          (source, origin, token) => {
+            bridge.createChannel(source, origin, token);
+            resolve();
+          },
+          [frame]
+        );
+      });
+    };
+
     /**
      * Remove the connection between the sidebar and annotator.
      */
diff --git a/src/annotator/index.js b/src/annotator/index.js
index c88e0f28125..c4aef38e63a 100644
--- a/src/annotator/index.js
+++ b/src/annotator/index.js
@@ -34,16 +34,11 @@ const appLinkEl = /** @type {Element} */ (
 );
 
 function init() {
+  window_.__hypothesis = {};
+
   const annotatorConfig = getConfig('annotator');
   const isPDF = typeof window_.PDFViewerApplication !== 'undefined';
 
-  if (annotatorConfig.subFrameIdentifier) {
-    // Other modules use this to detect if this
-    // frame context belongs to hypothesis.
-    // Needs to be a global property that's set.
-    window_.__hypothesis_frame = true;
-  }
-
   const eventBus = new EventBus();
   const guest = new Guest(document.body, eventBus, {
     ...annotatorConfig,
@@ -51,15 +46,37 @@ function init() {
     // nb. documentType is an internal config property only
     documentType: isPDF ? 'pdf' : 'html',
   });
+
   const sidebar = !annotatorConfig.subFrameIdentifier
     ? new Sidebar(document.body, eventBus, guest, getConfig('sidebar'))
     : null;
+  if (sidebar) {
+    // Expose sidebar window reference for use by same-origin guest frames.
+    window_.__hypothesis.sidebarWindow = sidebar.sidebarWindow;
+  }
+
   // Clear `annotations` value from the notebook's config to prevent direct-linked
   // annotations from filtering the threads.
   const notebook = new Notebook(document.body, eventBus, getConfig('notebook'));
 
+  // Setup guest <-> sidebar communication.
+  const sidebarWindow = sidebar
+    ? sidebar.sidebarWindow
+    : /** @type {HypothesisWindow} */ (window.parent).__hypothesis
+        ?.sidebarWindow;
+  if (sidebarWindow) {
+    guest.crossframe.connectToSidebar(sidebarWindow);
+  } else {
+    // eslint-disable-next-line no-console
+    console.warn(
+      `Hypothesis guest frame in ${location.origin} could not find a sidebar to connect to`
+    );
+  }
+
   appLinkEl.addEventListener('destroy', () => {
+    delete window_.__hypothesis;
     sidebar?.destroy();
+
     notebook.destroy();
     guest.destroy();
 
diff --git a/src/annotator/sidebar.js b/src/annotator/sidebar.js
index 9c35950f682..78c8c3c3f49 100644
--- a/src/annotator/sidebar.js
+++ b/src/annotator/sidebar.js
@@ -192,6 +192,13 @@ export default class Sidebar {
     this._setupSidebarEvents();
   }
 
+  /**
+   * Return a reference to the `Window` containing the sidebar application.
+   */
+  get sidebarWindow() {
+    return /** @type {Window} */ (this.iframe.contentWindow);
+  }
+
   destroy() {
     this.bucketBar?.destroy();
     this._listeners.removeAll();
diff --git a/src/annotator/test/integration/multi-frame-test.js b/src/annotator/test/integration/multi-frame-test.js
index 4dce8a287e6..caa6d066696 100644
--- a/src/annotator/test/integration/multi-frame-test.js
+++ b/src/annotator/test/integration/multi-frame-test.js
@@ -137,7 +137,7 @@ describe('CrossFrame multi-frame scenario', () => {
     const frame = document.createElement('iframe');
     frame.setAttribute('enable-annotation', '');
     container.appendChild(frame);
-    frame.contentWindow.eval('window.__hypothesis_frame = true');
+    frame.contentWindow.eval('window.__hypothesis = {}');
 
     crossFrame = createCrossFrame();
 
diff --git a/src/annotator/util/frame-util.js b/src/annotator/util/frame-util.js
index 3f896a86cac..b64be6b5555 100644
--- a/src/annotator/util/frame-util.js
+++ b/src/annotator/util/frame-util.js
@@ -17,7 +17,7 @@ export function findFrames(container) {
 
 // Check if the iframe has already been injected
 export function hasHypothesis(iframe) {
-  return iframe.contentWindow.__hypothesis_frame === true;
+  return '__hypothesis' in iframe.contentWindow;
 }
 
 // Inject embed.js into the iframe
diff --git a/src/shared/discovery.js b/src/shared/discovery.js
index faa1297a886..327630c9f47 100644
--- a/src/shared/discovery.js
+++ b/src/shared/discovery.js
@@ -72,8 +72,9 @@ export default class Discovery {
    *
    * @param {DiscoveryCallback} onDiscovery - Callback to invoke with a token when
    *   another frame is discovered.
+   * @param {Window[]} frames - A list of frames to attempt to connect to.
    */
-  startDiscovery(onDiscovery) {
+  startDiscovery(onDiscovery, frames) {
     if (this.onDiscovery) {
       throw new Error(
         'Discovery is already in progress. Call stopDiscovery() first'
@@ -84,7 +85,14 @@ export default class Discovery {
 
     // Listen for messages from other frames.
     this._listeners.add(this.target, 'message', this._onMessage);
-    this._beacon();
+
+    // Ping specified other frames to tell them about the existence of this frame.
+    const beaconMessage = this.server
+      ? '__cross_frame_dhcp_offer'
+      : '__cross_frame_dhcp_discovery';
+    for (let frame of frames) {
+      frame.postMessage(beaconMessage, this.origin);
+    }
   }
 
   /**
@@ -95,33 +103,6 @@ export default class Discovery {
     this._listeners.removeAll();
   }
 
-  /**
-   * Send a message to other frames in the current window to inform them about
-   * the existence of this frame and tell them whether this frame is a client
-   * or server.
-   */
-  _beacon() {
-    let beaconMessage;
-    if (this.server) {
-      beaconMessage = '__cross_frame_dhcp_offer';
-    } else {
-      beaconMessage = '__cross_frame_dhcp_discovery';
-    }
-
-    // Perform a top-down, breadth-first traversal of frames in the current
-    // window and send messages to them.
-    const queue = [this.target.top];
-    while (queue.length > 0) {
-      const parent = /** @type {Window} */ (queue.shift());
-      if (parent !== this.target) {
-        parent.postMessage(beaconMessage, this.origin);
-      }
-      for (let i = 0; i < parent.frames.length; i++) {
-        queue.push(parent.frames[i]);
-      }
-    }
-  }
-
   /**
    * Handle a `MessageEvent` from another frame which _may_ be from a
    * `Discovery` instance.
diff --git a/src/sidebar/services/frame-sync.js b/src/sidebar/services/frame-sync.js
index 4a22a289808..1229c567945 100644
--- a/src/sidebar/services/frame-sync.js
+++ b/src/sidebar/services/frame-sync.js
@@ -236,7 +236,10 @@ export class FrameSyncService {
     };
 
     const discovery = new Discovery(window, { server: true });
-    discovery.startDiscovery(this._bridge.createChannel.bind(this._bridge));
+    discovery.startDiscovery(this._bridge.createChannel.bind(this._bridge), [
+      // Ping the host frame which is in most cases also the only guest.
+      window.parent,
+    ]);
     this._bridge.onConnect(addFrame);
 
     this._setupSyncToFrame();
diff --git a/src/types/annotator.js b/src/types/annotator.js
index 3c066475090..564b4ad3537 100644
--- a/src/types/annotator.js
+++ b/src/types/annotator.js
@@ -142,9 +142,8 @@
  * @typedef Globals
  * @prop {import('./pdfjs').PDFViewerApplication} [PDFViewerApplication] -
  *   PDF.js entry point. If set, triggers loading of PDF rather than HTML integration.
- * @prop {boolean} [__hypothesis_frame] -
- *   Flag used to indicate that the "annotator" part of Hypothesis is loaded in
- *   the current frame.
+ * @prop {object} [__hypothesis] - Internal data related to supporting guests in iframes
+ *   @prop {Window} [sidebarWindow] - The sidebar window that is active in this frame.
  */
 
 /**