diff --git a/Sources/AppDelegate.swift b/Sources/AppDelegate.swift
index 34aa3bc6..abe88d39 100644
--- a/Sources/AppDelegate.swift
+++ b/Sources/AppDelegate.swift
@@ -5910,6 +5910,11 @@ final class AppDelegate: NSObject, NSApplicationDelegate, UNUserNotificationCent
         updateController.checkForUpdates()
     }
 
+    func checkForUpdatesInCustomUI() {
+        updateViewModel.overrideState = nil
+        updateController.checkForUpdatesInCustomUI()
+    }
+
     func openWelcomeWorkspace() {
         guard let context = preferredMainWindowContextForWorkspaceCreation(event: nil, debugSource: "welcome") else {
             return
diff --git a/Sources/Update/UpdateController.swift b/Sources/Update/UpdateController.swift
index 3ac1394a..c5fd4ad0 100644
--- a/Sources/Update/UpdateController.swift
+++ b/Sources/Update/UpdateController.swift
@@ -208,6 +208,11 @@ class UpdateController {
         checkForUpdatesWhenReady(retries: readyRetryCount)
     }
 
+    /// Check for updates using the custom popover-based UI.
+    func checkForUpdatesInCustomUI() {
+        checkForUpdatesWhenReady(retries: readyRetryCount)
+    }
+
     private func performCheckForUpdates() {
         startUpdaterIfNeeded()
         ensureSparkleInstallationCache()
diff --git a/Sources/Update/UpdatePill.swift b/Sources/Update/UpdatePill.swift
index 42abf9f8..25f163b2 100644
--- a/Sources/Update/UpdatePill.swift
+++ b/Sources/Update/UpdatePill.swift
@@ -28,8 +28,12 @@ struct UpdatePill: View {
     private var pillButton: some View {
         Button(action: {
             if model.showsDetectedBackgroundUpdate {
-                showPopover = false
-                AppDelegate.shared?.checkForUpdates(nil)
+                if showPopover {
+                    showPopover = false
+                } else {
+                    showPopover = true
+                    AppDelegate.shared?.checkForUpdatesInCustomUI()
+                }
                 return
             }
             if case .notFound(let notFound) = model.state {
diff --git a/Sources/Update/UpdatePopoverView.swift b/Sources/Update/UpdatePopoverView.swift
index 2361775d..301c3ae1 100644
--- a/Sources/Update/UpdatePopoverView.swift
+++ b/Sources/Update/UpdatePopoverView.swift
@@ -11,7 +11,12 @@ struct UpdatePopoverView: View {
         VStack(alignment: .leading, spacing: 0) {
             switch model.effectiveState {
             case .idle:
-                EmptyView()
+                if let detectedVersion = model.detectedUpdateVersion,
+                   model.showsDetectedBackgroundUpdate {
+                    DetectedBackgroundUpdateView(version: detectedVersion)
+                } else {
+                    EmptyView()
+                }
 
             case .permissionRequest(let request):
                 PermissionRequestView(request: request, dismiss: dismiss)
@@ -42,6 +47,35 @@ struct UpdatePopoverView: View {
     }
 }
 
+fileprivate struct DetectedBackgroundUpdateView: View {
+    let version: String
+
+    var body: some View {
+        VStack(alignment: .leading, spacing: 16) {
+            VStack(alignment: .leading, spacing: 8) {
+                Text(String(localized: "update.popover.updateAvailable", defaultValue: "Update Available"))
+                    .font(.system(size: 13, weight: .semibold))
+
+                HStack(spacing: 6) {
+                    Text(String(localized: "update.popover.version", defaultValue: "Version:"))
+                        .foregroundColor(.secondary)
+                        .frame(width: 60, alignment: .trailing)
+                    Text(version)
+                }
+                .font(.system(size: 11))
+            }
+
+            HStack(spacing: 10) {
+                ProgressView()
+                    .controlSize(.small)
+                Text(String(localized: "update.popover.checking", defaultValue: "Checking for updates…"))
+                    .font(.system(size: 13))
+            }
+        }
+        .padding(16)
+    }
+}
+
 fileprivate struct PermissionRequestView: View {
     let request: UpdateState.PermissionRequest
     let dismiss: DismissAction
diff --git a/cmuxUITests/UpdatePillUITests.swift b/cmuxUITests/UpdatePillUITests.swift
index d76c40ba..8493a0de 100644
--- a/cmuxUITests/UpdatePillUITests.swift
+++ b/cmuxUITests/UpdatePillUITests.swift
@@ -59,6 +59,32 @@ final class UpdatePillUITests: XCTestCase {
         attachScreenshot(name: "background-detected-update-available")
     }
 
+    func testDetectedBackgroundUpdateFirstClickOpensPopover() {
+        let systemSettings = XCUIApplication(bundleIdentifier: "com.apple.systempreferences")
+        systemSettings.terminate()
+
+        let app = XCUIApplication()
+        app.launchEnvironment["CMUX_UI_TEST_MODE"] = "1"
+        app.launchEnvironment["CMUX_UI_TEST_DETECTED_UPDATE_VERSION"] = "9.9.9"
+        app.launchEnvironment["CMUX_UI_TEST_FEED_URL"] = "https://cmux.test/appcast.xml"
+        app.launchEnvironment["CMUX_UI_TEST_FEED_MODE"] = "available"
+        app.launchEnvironment["CMUX_UI_TEST_UPDATE_VERSION"] = "9.9.9"
+        app.launchEnvironment["CMUX_UI_TEST_AUTO_ALLOW_PERMISSION"] = "1"
+        launchAndActivate(app)
+
+        let pill = pillButton(app: app, expectedLabel: "Update Available: 9.9.9")
+        XCTAssertTrue(pill.waitForExistence(timeout: 6.0))
+        assertVisibleSize(pill)
+
+        pill.click()
+
+        XCTAssertTrue(
+            app.staticTexts["Update Available"].waitForExistence(timeout: 8.0),
+            "Expected the first click on a background-detected update pill to open the popover"
+        )
+        XCTAssertTrue(app.buttons["Install and Relaunch"].waitForExistence(timeout: 2.0))
+    }
+
     func testUpdatePillShowsForNoUpdateThenDismisses() {
         let systemSettings = XCUIApplication(bundleIdentifier: "com.apple.systempreferences")
         systemSettings.terminate()