diff --git a/e2e-tests/cypress/tests/integration/channels/keyboard_shortcuts/shift_up_focuses_on_rhs_spec.js b/e2e-tests/cypress/tests/integration/channels/keyboard_shortcuts/shift_up_focuses_on_rhs_spec.js
index 125fbe5cfc..69e6928319 100644
--- a/e2e-tests/cypress/tests/integration/channels/keyboard_shortcuts/shift_up_focuses_on_rhs_spec.js
+++ b/e2e-tests/cypress/tests/integration/channels/keyboard_shortcuts/shift_up_focuses_on_rhs_spec.js
@@ -21,7 +21,7 @@ describe('Keyboard Shortcuts', () => {
 
     it('MM-T1277 SHIFT+UP', () => {
         // # Press shift+up to open the latest thread in the channel in the RHS
-        cy.uiGetPostTextBox().type('{shift}{uparrow}');
+        cy.uiGetPostTextBox().type('{shift+uparrow}', {delay: 50});
 
         // * RHS Opens up
         cy.get('.sidebar--right__header').should('be.visible');
@@ -33,7 +33,28 @@ describe('Keyboard Shortcuts', () => {
         cy.uiGetPostTextBox().click();
 
         // # Press shift+up again
-        cy.uiGetPostTextBox().type('{shift}{uparrow}');
+        cy.uiGetPostTextBox().type('{shift+uparrow}', {delay: 50});
+
+        // * RHS textbox should be focused
+        cy.uiGetReplyTextBox().should('be.focused');
+
+        // # Post a reply in the thread
+        cy.uiGetReplyTextBox().type('This is a reply{enter}');
+
+        // # Close the RHS by clicking the X button
+        cy.get('#rhsCloseButton').click();
+
+        // * Verify RHS is closed
+        cy.get('.sidebar--right__header').should('not.exist');
+
+        // # Click into the center channel post textbox
+        cy.uiGetPostTextBox().click();
+
+        // # Press shift+up to open the thread with replies
+        cy.uiGetPostTextBox().type('{shift+uparrow}', {delay: 50});
+
+        // * RHS Opens up
+        cy.get('.sidebar--right__header').should('be.visible');
 
         // * RHS textbox should be focused
         cy.uiGetReplyTextBox().should('be.focused');
diff --git a/e2e-tests/cypress/tests/integration/channels/messaging/focus_move_spec.js b/e2e-tests/cypress/tests/integration/channels/messaging/focus_move_spec.js
index 77d2e46666..41ba26aabf 100644
--- a/e2e-tests/cypress/tests/integration/channels/messaging/focus_move_spec.js
+++ b/e2e-tests/cypress/tests/integration/channels/messaging/focus_move_spec.js
@@ -15,12 +15,14 @@ import * as TIMEOUTS from '../../../fixtures/timeouts';
 describe('Messaging', () => {
     let offTopicUrl;
     let testChannelName;
+    let user;
 
     before(() => {
         // # Login as test user
         cy.apiInitSetup({loginAfter: true}).then((out) => {
             offTopicUrl = out.offTopicUrl;
             testChannelName = out.channel.display_name;
+            user = out.user;
         });
     });
 
@@ -97,6 +99,43 @@ describe('Messaging', () => {
         cy.uiGetReplyTextBox().should('be.focused');
     });
 
+    it('MM-T205 Focus to remain in RHS textbox when replying to reply post in center channel (CRT disabled)', () => {
+        // # Ensure collapsed reply threads is disabled
+        cy.apiSaveCRTPreference(user.id, 'off');
+
+        // # Post a thread root message
+        cy.postMessage('Thread root message');
+
+        // # Open RHS and post a reply
+        cy.clickPostCommentIcon();
+        cy.uiGetReplyTextBox().type('First reply{enter}');
+
+        // # Close RHS
+        cy.get('#rhsCloseButton').click();
+
+        // * Verify RHS is closed
+        cy.get('.sidebar--right__header').should('not.exist');
+
+        // # Get the reply post ID and click its comment icon
+        cy.getLastPostId().then((postId) => {
+            // # Click the reply arrow on the reply post
+            cy.clickPostCommentIcon(postId);
+
+            // * Verify RHS opens and textbox is focused
+            cy.get('.sidebar--right__header').should('be.visible');
+            cy.uiGetReplyTextBox().should('be.focused');
+
+            // # Focus away from RHS textbox
+            cy.get('#rhsContainer .post-right__content').click();
+
+            // # Click reply arrow on the same reply post again
+            cy.clickPostCommentIcon(postId);
+        });
+
+        // * Verify RHS textbox is focused again
+        cy.uiGetReplyTextBox().should('be.focused');
+    });
+
     it('MM-T203 Focus does not move when it has already been set elsewhere', () => {
         // # Verify Focus in add channel member modal
         verifyFocusInAddChannelMemberModal();
@@ -157,8 +196,8 @@ function verifyFocusInAddChannelMemberModal() {
     // * Check that input box has character A
     cy.get('#selectItems input').should('have.value', 'A');
 
-    // # Click anywhere in the modal that is not on a field that can take focus
-    cy.get('#deletePostModalLabel > span').click();
+    // # Remove the focus from the input box
+    cy.get('#selectItems input').blur();
 
     // * Note the focus has been removed from the search box
     cy.get('#selectItems input').should('not.be.focused');
diff --git a/webapp/channels/src/components/advanced_text_editor/advanced_text_editor.test.tsx b/webapp/channels/src/components/advanced_text_editor/advanced_text_editor.test.tsx
index daa9e29f62..64da39c015 100644
--- a/webapp/channels/src/components/advanced_text_editor/advanced_text_editor.test.tsx
+++ b/webapp/channels/src/components/advanced_text_editor/advanced_text_editor.test.tsx
@@ -236,7 +236,9 @@ describe('components/avanced_text_editor/advanced_text_editor', () => {
             expect(textbox).not.toHaveFocus();
 
             // save is called with a short delayed after pressing escape key
-            jest.advanceTimersByTime(Constants.SAVE_DRAFT_TIMEOUT + 50);
+            act(() => {
+                jest.advanceTimersByTime(Constants.SAVE_DRAFT_TIMEOUT + 50);
+            });
             expect(mockedRemoveDraft).toHaveBeenCalled();
             expect(mockedUpdateDraft).not.toHaveBeenCalled();
         });
diff --git a/webapp/channels/src/components/advanced_text_editor/use_textbox_focus.tsx b/webapp/channels/src/components/advanced_text_editor/use_textbox_focus.tsx
index 01ef01da4d..aaefb654ee 100644
--- a/webapp/channels/src/components/advanced_text_editor/use_textbox_focus.tsx
+++ b/webapp/channels/src/components/advanced_text_editor/use_textbox_focus.tsx
@@ -33,11 +33,20 @@ const useTextboxFocus = (
     const focusTextbox = useCallback((keepFocus = false) => {
         const postTextboxDisabled = !canPost;
         if (textboxRef.current && postTextboxDisabled) {
-            textboxRef.current.blur(); // Fixes Firefox bug which causes keyboard shortcuts to be ignored (MM-22482)
+            // Fixes Firefox bug which causes keyboard shortcuts to be ignored (MM-22482)
+            requestAnimationFrame(() => {
+                textboxRef.current?.blur();
+            });
             return;
         }
         if (textboxRef.current && (keepFocus || !UserAgent.isMobile())) {
-            textboxRef.current.focus();
+            // Focus immediately, so we capture any typed text.
+            textboxRef.current?.focus();
+
+            // Also re-focus after the next animation frame, to work around issues where the RHS is "opening".
+            requestAnimationFrame(() => {
+                textboxRef.current?.focus();
+            });
         }
     }, [canPost, textboxRef]);