diff --git a/web/packages/teleterm/src/ui/services/modals/modalsService.ts b/web/packages/teleterm/src/ui/services/modals/modalsService.ts
index d457a99f076c8..cbb293b73caea 100644
--- a/web/packages/teleterm/src/ui/services/modals/modalsService.ts
+++ b/web/packages/teleterm/src/ui/services/modals/modalsService.ts
@@ -52,11 +52,13 @@ export class ModalsService extends ImmutableStore<State> {
    *
    * Calling openRegularDialog while another regular dialog is displayed will simply overwrite the
    * old dialog with the new one.
+   * The old dialog is canceled, if possible.
    *
    * The returned closeDialog function can be used to close the dialog and automatically call the
    * dialog's onCancel callback (if present).
    */
   openRegularDialog(dialog: Dialog): { closeDialog: () => void } {
+    this.state.regular['onCancel']?.();
     this.setState(draftState => {
       draftState.regular = dialog;
     });
@@ -80,11 +82,13 @@ export class ModalsService extends ImmutableStore<State> {
    *
    * Calling openImportantDialog while another important dialog is displayed will simply overwrite
    * the old dialog with the new one.
+   * The old dialog is canceled, if possible.
    *
    * The returned closeDialog function can be used to close the dialog and automatically call the
    * dialog's onCancel callback (if present).
    */
   openImportantDialog(dialog: Dialog): { closeDialog: () => void } {
+    this.state.important['onCancel']?.();
     this.setState(draftState => {
       draftState.important = dialog;
     });
diff --git a/web/packages/teleterm/src/ui/utils/retryWithRelogin.test.ts b/web/packages/teleterm/src/ui/utils/retryWithRelogin.test.ts
index ec403000bba37..4096100f6ea36 100644
--- a/web/packages/teleterm/src/ui/utils/retryWithRelogin.test.ts
+++ b/web/packages/teleterm/src/ui/utils/retryWithRelogin.test.ts
@@ -16,6 +16,8 @@
  * along with this program.  If not, see <http://www.gnu.org/licenses/>.
  */
 
+import { waitFor } from '@testing-library/react';
+
 import { MockAppContext } from 'teleterm/ui/fixtures/mocks';
 import Logger, { NullService } from 'teleterm/logger';
 
@@ -166,3 +168,72 @@ it('calls actionToRetry again if relogin attempt was canceled', async () => {
   expect(actionToRetry).toHaveBeenCalledTimes(2);
   expect(actualReturnValue).toEqual(expectedReturnValue);
 });
+
+it('concurrent requests wait for the single login modal to resolve', async () => {
+  const appContext = new MockAppContext();
+
+  let logIn: () => void;
+  jest
+    .spyOn(appContext.modalsService, 'openRegularDialog')
+    .mockImplementation(dialog => {
+      if (dialog.kind === 'cluster-connect') {
+        logIn = () => dialog.onSuccess('/clusters/foo');
+      } else {
+        throw new Error(`Got unexpected dialog ${dialog.kind}`);
+      }
+
+      // Dialog cancel function.
+      return {
+        closeDialog: () => {},
+      };
+    });
+
+  jest
+    .spyOn(appContext.workspacesService, 'doesResourceBelongToActiveWorkspace')
+    .mockImplementation(() => true);
+
+  const firstExpectedReturnValue = Symbol('firstExpectedReturnValue');
+  const secondExpectedReturnValue = Symbol('secondExpectedReturnValue');
+  const firstActionToRetry = jest
+    .fn()
+    .mockRejectedValueOnce(makeRetryableError())
+    .mockResolvedValueOnce(firstExpectedReturnValue);
+  const secondActionToRetry = jest
+    .fn()
+    .mockRejectedValueOnce(makeRetryableError())
+    .mockResolvedValueOnce(secondExpectedReturnValue);
+
+  const firstAction = retryWithRelogin(
+    appContext,
+    '/clusters/foo/servers/bar',
+    firstActionToRetry
+  );
+  const secondAction = retryWithRelogin(
+    appContext,
+    '/clusters/foo/servers/xyz',
+    secondActionToRetry
+  );
+
+  const openRegularDialogSpy = appContext.modalsService.openRegularDialog;
+  await waitFor(() => {
+    expect(openRegularDialogSpy).toHaveBeenCalledTimes(1);
+  });
+  expect(openRegularDialogSpy).toHaveBeenCalledWith(
+    expect.objectContaining({
+      kind: 'cluster-connect',
+      clusterUri: '/clusters/foo',
+    })
+  );
+
+  logIn();
+
+  const firstActionExpectedReturnValue = await firstAction;
+  const secondActionExpectedReturnValue = await secondAction;
+
+  expect(firstActionToRetry).toHaveBeenCalledTimes(2);
+  expect(secondActionToRetry).toHaveBeenCalledTimes(2);
+  expect(firstActionExpectedReturnValue).toEqual(firstExpectedReturnValue);
+  expect(secondActionExpectedReturnValue).toEqual(secondExpectedReturnValue);
+
+  expect(openRegularDialogSpy).toHaveBeenCalledTimes(1);
+});
diff --git a/web/packages/teleterm/src/ui/utils/retryWithRelogin.ts b/web/packages/teleterm/src/ui/utils/retryWithRelogin.ts
index 5fcf4563764eb..5c05b7b0d733a 100644
--- a/web/packages/teleterm/src/ui/utils/retryWithRelogin.ts
+++ b/web/packages/teleterm/src/ui/utils/retryWithRelogin.ts
@@ -22,6 +22,8 @@ import Logger from 'teleterm/logger';
 
 const logger = new Logger('retryWithRelogin');
 
+let pendingLoginDialog: Promise<void> | undefined;
+
 /**
  * `retryWithRelogin` executes `actionToRetry`. If `actionToRetry` throws an error, it checks if the
  * error can be resolved by the user logging in, according to metadata returned from the tshd
@@ -31,6 +33,10 @@ const logger = new Logger('retryWithRelogin');
  * argument) and if so, it shows a login modal. After the user successfully logs in, it calls
  * `actionToRetry` again.
  *
+ * `retryWithRelogin` supports concurrent requests.
+ * If multiple actions need to show a login modal at the same time,
+ * it will be displayed only once, and other actions will wait for it to be resolved.
+ *
  * Each place using `retryWithRelogin` must be able to show the error to the user in case the
  * relogin attempt fails. Each place should also offer the user a way to manually retry the action
  * which results in a call to the tshd client.
@@ -75,7 +81,13 @@ export async function retryWithRelogin<T>(
 
   const rootClusterUri = routing.ensureRootClusterUri(resourceUri);
 
-  await login(appContext, rootClusterUri);
+  if (!pendingLoginDialog) {
+    pendingLoginDialog = login(appContext, rootClusterUri).finally(() => {
+      pendingLoginDialog = undefined;
+    });
+  }
+
+  await pendingLoginDialog;
 
   return await actionToRetry();
 }