diff --git a/remote/shared/messagehandler/MessageHandler.sys.mjs b/remote/shared/messagehandler/MessageHandler.sys.mjs
index 86eb2dc950aa..18ec6b820c36 100644
--- a/remote/shared/messagehandler/MessageHandler.sys.mjs
+++ b/remote/shared/messagehandler/MessageHandler.sys.mjs
@@ -263,15 +263,15 @@ export class MessageHandler extends EventEmitter {
   }
 
   /**
-   * Apply the initial session data items provided to this MessageHandler on
-   * startup. Implementation is specific to each MessageHandler class.
+   * Execute the required initialization steps, inlcluding apply the initial session data items
+   * provided to this MessageHandler on startup. Implementation is specific to each MessageHandler class.
    *
    * By default the implementation is a no-op.
    *
    * @param {Array<SessionDataItem>} sessionDataItems
    *     Initial session data items for this MessageHandler.
    */
-  async applyInitialSessionDataItems(sessionDataItems) {}
+  async initialize(sessionDataItems) {}
 
   /**
    * Returns the module path corresponding to this MessageHandler class.
diff --git a/remote/shared/messagehandler/MessageHandlerRegistry.sys.mjs b/remote/shared/messagehandler/MessageHandlerRegistry.sys.mjs
index 538f4bfc29bd..6a09173f5023 100644
--- a/remote/shared/messagehandler/MessageHandlerRegistry.sys.mjs
+++ b/remote/shared/messagehandler/MessageHandlerRegistry.sys.mjs
@@ -202,7 +202,7 @@ export class MessageHandlerRegistry extends EventEmitter {
     );
     messageHandler.on("message-handler-event", this._onMessageHandlerEvent);
 
-    messageHandler.applyInitialSessionDataItems(sessionDataItems);
+    messageHandler.initialize(sessionDataItems);
 
     this._messageHandlersMap.set(sessionId, messageHandler);
 
diff --git a/remote/shared/messagehandler/RootMessageHandler.sys.mjs b/remote/shared/messagehandler/RootMessageHandler.sys.mjs
index aef945d15f46..e3c2652927fe 100644
--- a/remote/shared/messagehandler/RootMessageHandler.sys.mjs
+++ b/remote/shared/messagehandler/RootMessageHandler.sys.mjs
@@ -25,6 +25,7 @@ ChromeUtils.defineESModuleGetters(lazy, {
  */
 export class RootMessageHandler extends MessageHandler {
   #navigationManager;
+  #realms;
   #rootTransport;
   #sessionData;
 
@@ -67,12 +68,25 @@ export class RootMessageHandler extends MessageHandler {
     this.#sessionData = new lazy.SessionData(this);
     this.#navigationManager = new lazy.NavigationManager();
     this.#navigationManager.startMonitoring();
+
+    // Map with inner window ids as keys, and sets of realm ids, assosiated with
+    // this window as values.
+    this.#realms = new Map();
+    // In the general case, we don't get notified that realms got destroyed,
+    // because there is no communication between content and parent process at this moment,
+    // so we have to listen to the this notification to clean up the internal
+    // map and trigger the events.
+    Services.obs.addObserver(this, "window-global-destroyed");
   }
 
   get navigationManager() {
     return this.#navigationManager;
   }
 
+  get realms() {
+    return this.#realms;
+  }
+
   get sessionData() {
     return this.#sessionData;
   }
@@ -80,6 +94,10 @@ export class RootMessageHandler extends MessageHandler {
   destroy() {
     this.#sessionData.destroy();
     this.#navigationManager.destroy();
+
+    Services.obs.removeObserver(this, "window-global-destroyed");
+    this.#realms = null;
+
     super.destroy();
   }
 
@@ -96,6 +114,22 @@ export class RootMessageHandler extends MessageHandler {
     return this.updateSessionData([sessionData]);
   }
 
+  emitEvent(name, eventPayload, contextInfo) {
+    // Intercept realm created and destroyed events to update internal map.
+    if (name === "realm-created") {
+      this.#onRealmCreated(eventPayload);
+    }
+    // We receive this events in the case of moving the page to BFCache.
+    if (name === "windowglobal-pagehide") {
+      this.#cleanUpRealmsForWindow(
+        eventPayload.innerWindowId,
+        eventPayload.context
+      );
+    }
+
+    super.emitEvent(name, eventPayload, contextInfo);
+  }
+
   /**
    * Emit a public protocol event. This event will be sent over to the client.
    *
@@ -137,6 +171,17 @@ export class RootMessageHandler extends MessageHandler {
     return true;
   }
 
+  observe(subject, topic) {
+    if (topic !== "window-global-destroyed") {
+      return;
+    }
+
+    this.#cleanUpRealmsForWindow(
+      subject.innerWindowId,
+      subject.browsingContext
+    );
+  }
+
   /**
    * Remove session data items of a given module, category and
    * contextDescriptor.
@@ -160,4 +205,33 @@ export class RootMessageHandler extends MessageHandler {
   async updateSessionData(sessionData = []) {
     await this.#sessionData.updateSessionData(sessionData);
   }
+
+  #cleanUpRealmsForWindow(innerWindowId, context) {
+    const realms = this.#realms.get(innerWindowId);
+
+    if (!realms) {
+      return;
+    }
+
+    realms.forEach(realm => {
+      this.#realms.get(innerWindowId).delete(realm);
+
+      this.emitEvent("realm-destroyed", {
+        context,
+        realm,
+      });
+    });
+
+    this.#realms.delete(innerWindowId);
+  }
+
+  #onRealmCreated = data => {
+    const { innerWindowId, realmId } = data;
+
+    if (!this.#realms.has(innerWindowId)) {
+      this.#realms.set(innerWindowId, new Set());
+    }
+
+    this.#realms.get(innerWindowId).add(realmId);
+  };
 }
diff --git a/remote/shared/messagehandler/WindowGlobalMessageHandler.sys.mjs b/remote/shared/messagehandler/WindowGlobalMessageHandler.sys.mjs
index 1e0164cf44fe..d2ec6024ae47 100644
--- a/remote/shared/messagehandler/WindowGlobalMessageHandler.sys.mjs
+++ b/remote/shared/messagehandler/WindowGlobalMessageHandler.sys.mjs
@@ -34,15 +34,33 @@ export class WindowGlobalMessageHandler extends MessageHandler {
 
     this.#innerWindowId = this.context.window.windowGlobalChild.innerWindowId;
 
-    // Maps sandbox names to instances of window realms,
-    // the default realm is mapped to an empty string sandbox name.
-    this.#realms = new Map([["", new lazy.WindowRealm(this.context.window)]]);
+    // Maps sandbox names to instances of window realms.
+    this.#realms = new Map();
+  }
+
+  initialize(sessionDataItems) {
+    // Create the default realm, it is mapped to an empty string sandbox name.
+    this.#realms.set("", this.#createRealm());
+
+    // This method, even though being async, is not awaited on purpose,
+    // since for now the sessionDataItems are passed in response to an event in a for loop.
+    this.#applyInitialSessionDataItems(sessionDataItems);
+
+    // With the session data applied the handler is now ready to be used.
+    this.emitEvent("window-global-handler-created", {
+      contextId: this.contextId,
+      innerWindowId: this.#innerWindowId,
+    });
   }
 
   destroy() {
     for (const realm of this.#realms.values()) {
       realm.destroy();
     }
+    this.emitEvent("windowglobal-pagehide", {
+      context: this.context,
+      innerWindowId: this.innerWindowId,
+    });
     this.#realms = null;
 
     super.destroy();
@@ -92,6 +110,19 @@ export class WindowGlobalMessageHandler extends MessageHandler {
     return this.context.window;
   }
 
+  #createRealm(sandboxName = null) {
+    const realm = new lazy.WindowRealm(this.context.window, {
+      sandboxName,
+    });
+
+    this.emitEvent("realm-created", {
+      realmId: realm.id,
+      innerWindowId: this.innerWindowId,
+    });
+
+    return realm;
+  }
+
   #getRealmFromSandboxName(sandboxName = null) {
     if (sandboxName === null || sandboxName === "") {
       return this.#realms.get("");
@@ -101,16 +132,14 @@ export class WindowGlobalMessageHandler extends MessageHandler {
       return this.#realms.get(sandboxName);
     }
 
-    const realm = new lazy.WindowRealm(this.context.window, {
-      sandboxName,
-    });
+    const realm = this.#createRealm(sandboxName);
 
     this.#realms.set(sandboxName, realm);
 
     return realm;
   }
 
-  async applyInitialSessionDataItems(sessionDataItems) {
+  async #applyInitialSessionDataItems(sessionDataItems) {
     if (!Array.isArray(sessionDataItems)) {
       return;
     }
@@ -163,12 +192,6 @@ export class WindowGlobalMessageHandler extends MessageHandler {
     }
 
     await Promise.all(sessionDataPromises);
-
-    // With the session data applied the handler is now ready to be used.
-    this.emitEvent("window-global-handler-created", {
-      contextId: this.contextId,
-      innerWindowId: this.#innerWindowId,
-    });
   }
 
   forwardCommand(command) {
diff --git a/remote/shared/messagehandler/test/browser/browser.ini b/remote/shared/messagehandler/test/browser/browser.ini
index 8a3cc19d8b56..c603b63a3e3e 100644
--- a/remote/shared/messagehandler/test/browser/browser.ini
+++ b/remote/shared/messagehandler/test/browser/browser.ini
@@ -16,6 +16,7 @@ prefs =
 [browser_handle_command_retry.js]
 [browser_handle_simple_command.js]
 [browser_navigation_manager.js]
+[browser_realms.js]
 [browser_registry.js]
 [browser_session_data.js]
 [browser_session_data_browser_element.js]
diff --git a/remote/shared/messagehandler/test/browser/browser_events_module.js b/remote/shared/messagehandler/test/browser/browser_events_module.js
index 536c1d9754a3..32b60d34b14f 100644
--- a/remote/shared/messagehandler/test/browser/browser_events_module.js
+++ b/remote/shared/messagehandler/test/browser/browser_events_module.js
@@ -24,19 +24,38 @@ add_task(async function test_event() {
   const browsingContext = tab.linkedBrowser.browsingContext;
 
   const rootMessageHandler = createRootMessageHandler("session-id-event");
+  let messageHandlerEvent;
+  let registryEvent;
 
   // Events are emitted both as generic message-handler-event events as well
   // as under their own name. We expect to receive the event for both.
-  const onHandlerEvent = rootMessageHandler.once("message-handler-event");
+  const _onMessageHandlerEvent = (eventName, eventData) => {
+    if (eventData.name === "event-from-window-global") {
+      messageHandlerEvent = eventData;
+    }
+  };
+  rootMessageHandler.on("message-handler-event", _onMessageHandlerEvent);
   const onNamedEvent = rootMessageHandler.once("event-from-window-global");
   // MessageHandlerRegistry should forward all the message-handler-events.
-  const onRegistryEvent = RootMessageHandlerRegistry.once(
-    "message-handler-registry-event"
+  const _onMessageHandlerRegistryEvent = (eventName, eventData) => {
+    if (eventData.name === "event-from-window-global") {
+      registryEvent = eventData;
+    }
+  };
+  RootMessageHandlerRegistry.on(
+    "message-handler-registry-event",
+    _onMessageHandlerRegistryEvent
   );
 
   callTestEmitEvent(rootMessageHandler, browsingContext.id);
 
-  const messageHandlerEvent = await onHandlerEvent;
+  const namedEvent = await onNamedEvent;
+  is(
+    namedEvent.text,
+    `event from ${browsingContext.id}`,
+    "Received the expected payload"
+  );
+
   is(
     messageHandlerEvent.name,
     "event-from-window-global",
@@ -48,20 +67,16 @@ add_task(async function test_event() {
     "Received the expected payload"
   );
 
-  const namedEvent = await onNamedEvent;
-  is(
-    namedEvent.text,
-    `event from ${browsingContext.id}`,
-    "Received the expected payload"
-  );
-
-  const registryEvent = await onRegistryEvent;
   is(
     registryEvent,
     messageHandlerEvent,
     "The event forwarded by the MessageHandlerRegistry is identical to the MessageHandler event"
   );
-
+  rootMessageHandler.off("message-handler-event", _onMessageHandlerEvent);
+  RootMessageHandlerRegistry.off(
+    "message-handler-registry-event",
+    _onMessageHandlerRegistryEvent
+  );
   rootMessageHandler.destroy();
   gBrowser.removeTab(tab);
 });
diff --git a/remote/shared/messagehandler/test/browser/browser_realms.js b/remote/shared/messagehandler/test/browser/browser_realms.js
new file mode 100644
index 000000000000..2ec98ca08dc9
--- /dev/null
+++ b/remote/shared/messagehandler/test/browser/browser_realms.js
@@ -0,0 +1,152 @@
+/* Any copyright is dedicated to the Public Domain.
+ * http://creativecommons.org/publicdomain/zero/1.0/ */
+
+"use strict";
+
+const { RootMessageHandler } = ChromeUtils.importESModule(
+  "chrome://remote/content/shared/messagehandler/RootMessageHandler.sys.mjs"
+);
+
+add_task(async function test_tab_is_removed() {
+  const tab = await addTab("https://example.com/document-builder.sjs?html=tab");
+  const sessionId = "realms";
+  const browsingContext = tab.linkedBrowser.browsingContext;
+  const contextDescriptor = {
+    type: ContextDescriptorType.TopBrowsingContext,
+    id: browsingContext.browserId,
+  };
+
+  const rootMessageHandler = createRootMessageHandler(sessionId);
+
+  const onRealmCreated = rootMessageHandler.once("realm-created");
+
+  // Add a new session data item to get window global handlers created
+  await rootMessageHandler.addSessionDataItem({
+    moduleName: "command",
+    category: "browser_realms",
+    contextDescriptor,
+    values: [true],
+  });
+
+  const realmCreatedEvent = await onRealmCreated;
+  const createdRealmId = realmCreatedEvent.realmId;
+
+  is(rootMessageHandler.realms.size, 1, "Realm is added in the internal map");
+
+  const onRealmDestroyed = rootMessageHandler.once("realm-destroyed");
+
+  gBrowser.removeTab(tab);
+
+  const realmDestroyedEvent = await onRealmDestroyed;
+
+  is(
+    realmDestroyedEvent.realm,
+    createdRealmId,
+    "Received a correct realm id in realm-destroyed event"
+  );
+  is(rootMessageHandler.realms.size, 0, "The realm map is cleaned up");
+
+  rootMessageHandler.destroy();
+});
+
+add_task(async function test_same_origin_navigation() {
+  const tab = await addTab("https://example.com/document-builder.sjs?html=tab");
+  const sessionId = "realms";
+  const browsingContext = tab.linkedBrowser.browsingContext;
+  const contextDescriptor = {
+    type: ContextDescriptorType.TopBrowsingContext,
+    id: browsingContext.browserId,
+  };
+
+  const rootMessageHandler = createRootMessageHandler(sessionId);
+
+  const onRealmCreated = rootMessageHandler.once("realm-created");
+
+  // Add a new session data item to get window global handlers created
+  await rootMessageHandler.addSessionDataItem({
+    moduleName: "command",
+    category: "browser_realms",
+    contextDescriptor,
+    values: [true],
+  });
+
+  const realmCreatedEvent = await onRealmCreated;
+  const createdRealmId = realmCreatedEvent.realmId;
+
+  is(rootMessageHandler.realms.size, 1, "Realm is added in the internal map");
+
+  const onRealmDestroyed = rootMessageHandler.once("realm-destroyed");
+  const onNewRealmCreated = rootMessageHandler.once("realm-created");
+
+  // Navigate to another page with the same origin
+  await loadURL(
+    tab.linkedBrowser,
+    "https://example.com/document-builder.sjs?html=othertab"
+  );
+
+  const realmDestroyedEvent = await onRealmDestroyed;
+
+  is(
+    realmDestroyedEvent.realm,
+    createdRealmId,
+    "Received a correct realm id in realm-destroyed event"
+  );
+
+  await onNewRealmCreated;
+
+  is(rootMessageHandler.realms.size, 1, "Realm is added in the internal map");
+
+  gBrowser.removeTab(tab);
+  rootMessageHandler.destroy();
+});
+
+add_task(async function test_cross_origin_navigation() {
+  const tab = await addTab("https://example.com/document-builder.sjs?html=tab");
+  const sessionId = "realms";
+  const browsingContext = tab.linkedBrowser.browsingContext;
+  const contextDescriptor = {
+    type: ContextDescriptorType.TopBrowsingContext,
+    id: browsingContext.browserId,
+  };
+
+  const rootMessageHandler = createRootMessageHandler(sessionId);
+
+  const onRealmCreated = rootMessageHandler.once("realm-created");
+
+  // Add a new session data item to get window global handlers created
+  await rootMessageHandler.addSessionDataItem({
+    moduleName: "command",
+    category: "browser_realms",
+    contextDescriptor,
+    values: [true],
+  });
+
+  const realmCreatedEvent = await onRealmCreated;
+  const createdRealmId = realmCreatedEvent.realmId;
+
+  is(rootMessageHandler.realms.size, 1, "Realm is added in the internal map");
+
+  const onRealmDestroyed = rootMessageHandler.once("realm-destroyed");
+  const onNewRealmCreated = rootMessageHandler.once("realm-created");
+
+  // Navigate to another page with the different origin
+  await loadURL(
+    tab.linkedBrowser,
+    "https://example.com/document-builder.sjs?html=otherorigin"
+  );
+
+  const realmDestroyedEvent = await onRealmDestroyed;
+
+  is(
+    realmDestroyedEvent.realm,
+    createdRealmId,
+    "Received a correct realm id in realm-destroyed event"
+  );
+
+  await onNewRealmCreated;
+
+  is(rootMessageHandler.realms.size, 1, "Realm is added in the internal map");
+
+  gBrowser.removeTab(tab);
+  rootMessageHandler.destroy();
+});
diff --git a/remote/shared/messagehandler/test/browser/browser_session_data.js b/remote/shared/messagehandler/test/browser/browser_session_data.js
index f0fef31883d5..17015e892d2c 100644
--- a/remote/shared/messagehandler/test/browser/browser_session_data.js
+++ b/remote/shared/messagehandler/test/browser/browser_session_data.js
@@ -186,7 +186,9 @@ add_task(async function test_sessionDataRootOnlyModule() {
     "https://example.com/document-builder.sjs?html=tab"
   );
 
-  const windowGlobalCreated = rootMessageHandler.once("message-handler-event");
+  const windowGlobalCreated = rootMessageHandler.once(
+    "window-global-handler-created"
+  );
 
   info("Test that adding SessionData items works the root module");
   // Updating the session data on the root message handler should not cause
diff --git a/remote/webdriver-bidi/modules/root/script.sys.mjs b/remote/webdriver-bidi/modules/root/script.sys.mjs
index 4c72621144cc..1adcc1d43270 100644
--- a/remote/webdriver-bidi/modules/root/script.sys.mjs
+++ b/remote/webdriver-bidi/modules/root/script.sys.mjs
@@ -40,6 +40,7 @@ const ScriptEvaluateResultType = {
 
 class ScriptModule extends Module {
   #preloadScriptMap;
+  #subscribedEvents;
 
   constructor(messageHandler) {
     super(messageHandler);
@@ -48,10 +49,14 @@ class ScriptModule extends Module {
     // with an item named expression, which is a string,
     // and an item named sandbox which is a string or null.
     this.#preloadScriptMap = new Map();
+
+    // Set of event names which have active subscriptions.
+    this.#subscribedEvents = new Set();
   }
 
   destroy() {
     this.#preloadScriptMap = null;
+    this.#subscribedEvents = null;
   }
 
   /**
@@ -746,8 +751,77 @@ class ScriptModule extends Module {
       .filter(realm => realm.context !== null);
   }
 
+  #onRealmDestroyed = (eventName, { realm, context }) => {
+    // This event is emitted from the parent process but for a given browsing
+    // context. Set the event's contextInfo to the message handler corresponding
+    // to this browsing context.
+    const contextInfo = {
+      contextId: context.id,
+      type: lazy.WindowGlobalMessageHandler.type,
+    };
+
+    this.emitEvent("script.realmDestroyed", { realm }, contextInfo);
+  };
+
+  #startListingOnRealmDestroyed() {
+    if (!this.#subscribedEvents.has("script.realmDestroyed")) {
+      this.messageHandler.on("realm-destroyed", this.#onRealmDestroyed);
+    }
+  }
+
+  #stopListingOnRealmDestroyed() {
+    if (this.#subscribedEvents.has("script.realmDestroyed")) {
+      this.messageHandler.off("realm-destroyed", this.#onRealmDestroyed);
+    }
+  }
+
+  #subscribeEvent(event) {
+    switch (event) {
+      case "script.realmDestroyed": {
+        this.#startListingOnRealmDestroyed();
+        this.#subscribedEvents.add(event);
+        break;
+      }
+    }
+  }
+
+  #unsubscribeEvent(event) {
+    switch (event) {
+      case "script.realmDestroyed": {
+        this.#stopListingOnRealmDestroyed();
+        this.#subscribedEvents.delete(event);
+        break;
+      }
+    }
+  }
+
+  _applySessionData(params) {
+    // TODO: Bug 1775231. Move this logic to a shared module or an abstract
+    // class.
+    const { category } = params;
+    if (category === "event") {
+      const filteredSessionData = params.sessionData.filter(item =>
+        this.messageHandler.matchesContext(item.contextDescriptor)
+      );
+      for (const event of this.#subscribedEvents.values()) {
+        const hasSessionItem = filteredSessionData.some(
+          item => item.value === event
+        );
+        // If there are no session items for this context, we should unsubscribe from the event.
+        if (!hasSessionItem) {
+          this.#unsubscribeEvent(event);
+        }
+      }
+
+      // Subscribe to all events, which have an item in SessionData.
+      for (const { value } of filteredSessionData) {
+        this.#subscribeEvent(value);
+      }
+    }
+  }
+
   static get supportedEvents() {
-    return ["script.message"];
+    return ["script.message", "script.realmDestroyed"];
   }
 }