diff --git a/coderd/httpapi/websocket.go b/coderd/httpapi/websocket.go
index b0c7e456b5..c483cf1834 100644
--- a/coderd/httpapi/websocket.go
+++ b/coderd/httpapi/websocket.go
@@ -3,20 +3,26 @@ package httpapi
 import (
 	"context"
 	"errors"
+	"net"
 	"time"
 
 	"golang.org/x/xerrors"
 
 	"cdr.dev/slog/v3"
+	"github.com/coder/quartz"
 	"github.com/coder/websocket"
 )
 
 const HeartbeatInterval time.Duration = 15 * time.Second
 
-// HeartbeatClose loops to ping a WebSocket to keep it alive. It calls `exit` on ping
-// failure.
+// HeartbeatClose loops to ping a WebSocket to keep it alive.
+// It calls `exit` on ping failure.
 func HeartbeatClose(ctx context.Context, logger slog.Logger, exit func(), conn *websocket.Conn) {
-	ticker := time.NewTicker(HeartbeatInterval)
+	heartbeatCloseWith(ctx, logger, exit, conn, quartz.NewReal(), HeartbeatInterval)
+}
+
+func heartbeatCloseWith(ctx context.Context, logger slog.Logger, exit func(), conn *websocket.Conn, clk quartz.Clock, interval time.Duration) {
+	ticker := clk.NewTicker(interval, "HeartbeatClose")
 	defer ticker.Stop()
 
 	for {
@@ -25,11 +31,21 @@ func HeartbeatClose(ctx context.Context, logger slog.Logger, exit func(), conn *
 			return
 		case <-ticker.C:
 		}
-		err := pingWithTimeout(ctx, conn, HeartbeatInterval)
+		err := pingWithTimeout(ctx, conn, interval)
 		if err != nil {
-			// context.DeadlineExceeded is expected when the client disconnects without sending a close frame.
-			// context.Canceled is expected when the request context is canceled.
-			if errors.Is(err, context.DeadlineExceeded) || errors.Is(err, context.Canceled) {
+			// These errors are all expected during normal connection
+			// teardown and should not be logged at error level:
+			//   - context.DeadlineExceeded: client disconnected
+			//     without sending a close frame.
+			//   - context.Canceled: request context was canceled.
+			//   - net.ErrClosed: connection was already closed by
+			//     another goroutine (e.g. handler returned).
+			//   - websocket.CloseError: a close frame was
+			//     received or sent.
+			if errors.Is(err, context.DeadlineExceeded) ||
+				errors.Is(err, context.Canceled) ||
+				errors.Is(err, net.ErrClosed) ||
+				websocket.CloseStatus(err) != -1 {
 				logger.Debug(ctx, "heartbeat ping stopped", slog.Error(err))
 			} else {
 				logger.Error(ctx, "failed to heartbeat ping", slog.Error(err))
diff --git a/coderd/httpapi/websocket_internal_test.go b/coderd/httpapi/websocket_internal_test.go
new file mode 100644
index 0000000000..09d18aa38e
--- /dev/null
+++ b/coderd/httpapi/websocket_internal_test.go
@@ -0,0 +1,210 @@
+package httpapi
+
+import (
+	"context"
+	"net/http"
+	"net/http/httptest"
+	"sync"
+	"testing"
+	"time"
+
+	"github.com/stretchr/testify/assert"
+	"github.com/stretchr/testify/require"
+
+	"cdr.dev/slog/v3"
+	"github.com/coder/coder/v2/testutil"
+	"github.com/coder/quartz"
+	"github.com/coder/websocket"
+)
+
+// logSink captures log entries so tests can assert on log levels.
+type logSink struct {
+	mu      sync.Mutex
+	entries []slog.SinkEntry
+}
+
+func (s *logSink) LogEntry(_ context.Context, e slog.SinkEntry) {
+	s.mu.Lock()
+	defer s.mu.Unlock()
+	s.entries = append(s.entries, e)
+}
+
+func (*logSink) Sync() {}
+
+func (s *logSink) entriesAtLevel(level slog.Level) []slog.SinkEntry {
+	s.mu.Lock()
+	defer s.mu.Unlock()
+	var result []slog.SinkEntry
+	for _, e := range s.entries {
+		if e.Level == level {
+			result = append(result, e)
+		}
+	}
+	return result
+}
+
+// websocketPair sets up an httptest server with a websocket endpoint and
+// returns the server-side conn. The server handler stays alive until ctx
+// is done.
+func websocketPair(ctx context.Context, t *testing.T) *websocket.Conn {
+	t.Helper()
+	serverConnCh := make(chan *websocket.Conn, 1)
+
+	srv := httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+		conn, err := websocket.Accept(w, r, nil)
+		if err != nil {
+			return
+		}
+		serverConnCh <- conn
+		// Keep the handler alive so the HTTP server doesn't close
+		// the connection from under us.
+		<-ctx.Done()
+	}))
+	t.Cleanup(srv.Close)
+
+	//nolint:bodyclose
+	clientConn, _, err := websocket.Dial(ctx, srv.URL, nil)
+	require.NoError(t, err)
+	t.Cleanup(func() {
+		_ = clientConn.Close(websocket.StatusNormalClosure, "test cleanup")
+	})
+
+	select {
+	case sc := <-serverConnCh:
+		return sc
+	case <-ctx.Done():
+		t.Fatal("timed out waiting for server websocket accept")
+		return nil
+	}
+}
+
+func TestHeartbeatClose(t *testing.T) {
+	t.Parallel()
+
+	t.Run("ServerSideClose", func(t *testing.T) {
+		t.Parallel()
+		ctx := testutil.Context(t, testutil.WaitShort)
+
+		sink := &logSink{}
+		logger := slog.Make(sink).Leveled(slog.LevelDebug)
+		mClock := quartz.NewMock(t)
+
+		// Trap ticker creation so we can synchronize startup.
+		trap := mClock.Trap().NewTicker("HeartbeatClose")
+		defer trap.Close()
+
+		serverConn := websocketPair(ctx, t)
+		exitCalled := make(chan struct{})
+
+		go heartbeatCloseWith(ctx, logger, func() {
+			close(exitCalled)
+		}, serverConn, mClock, time.Second)
+
+		// Wait for the ticker to be created, then release.
+		trap.MustWait(ctx).MustRelease(ctx)
+
+		// Close the server-side connection before the tick fires.
+		// The next ping will get net.ErrClosed.
+		_ = serverConn.Close(websocket.StatusGoingAway, "simulated teardown")
+
+		// Advance clock to trigger the tick.
+		mClock.Advance(time.Second).MustWait(ctx)
+
+		// Wait for heartbeatClose to call exit.
+		select {
+		case <-exitCalled:
+		case <-ctx.Done():
+			t.Fatal("timed out waiting for heartbeatClose to call exit")
+		}
+
+		// A closed connection is a normal shutdown condition. The
+		// error should be logged at Debug, not Error.
+		errorEntries := sink.entriesAtLevel(slog.LevelError)
+		assert.Empty(t, errorEntries,
+			"closed connection should not produce error-level logs, got: %+v", errorEntries)
+		debugEntries := sink.entriesAtLevel(slog.LevelDebug)
+		assert.NotEmpty(t, debugEntries,
+			"expected a debug-level log entry for the closed connection")
+	})
+
+	t.Run("ContextCanceled", func(t *testing.T) {
+		t.Parallel()
+		ctx := testutil.Context(t, testutil.WaitShort)
+
+		sink := &logSink{}
+		logger := slog.Make(sink).Leveled(slog.LevelDebug)
+		mClock := quartz.NewMock(t)
+
+		trap := mClock.Trap().NewTicker("HeartbeatClose")
+		defer trap.Close()
+
+		serverCtx, serverCancel := context.WithCancel(ctx)
+		serverConn := websocketPair(ctx, t)
+		done := make(chan struct{})
+
+		go func() {
+			defer close(done)
+			heartbeatCloseWith(serverCtx, logger, func() {
+				t.Error("exit should not be called on context cancel")
+			}, serverConn, mClock, time.Second)
+		}()
+
+		trap.MustWait(ctx).MustRelease(ctx)
+
+		// Cancel the context. HeartbeatClose should return via
+		// the <-ctx.Done() branch without calling exit.
+		serverCancel()
+
+		select {
+		case <-done:
+		case <-ctx.Done():
+			t.Fatal("timed out waiting for heartbeatClose to return")
+		}
+
+		errorEntries := sink.entriesAtLevel(slog.LevelError)
+		assert.Empty(t, errorEntries,
+			"context cancellation should not produce error-level logs, got: %+v", errorEntries)
+	})
+
+	t.Run("PingSucceeds", func(t *testing.T) {
+		t.Parallel()
+		ctx := testutil.Context(t, testutil.WaitShort)
+
+		sink := &logSink{}
+		logger := slog.Make(sink).Leveled(slog.LevelDebug)
+		mClock := quartz.NewMock(t)
+
+		trap := mClock.Trap().NewTicker("HeartbeatClose")
+		defer trap.Close()
+
+		serverConn := websocketPair(ctx, t)
+		exitCalled := make(chan struct{}, 1)
+
+		go heartbeatCloseWith(ctx, logger, func() {
+			exitCalled <- struct{}{}
+		}, serverConn, mClock, time.Second)
+
+		trap.MustWait(ctx).MustRelease(ctx)
+
+		// Fire several ticks — pings should succeed each time.
+		for range 3 {
+			mClock.Advance(time.Second).MustWait(ctx)
+
+			// Give the ping round-trip time to complete.
+			// If exit were called, we'd catch it.
+			select {
+			case <-exitCalled:
+				t.Fatal("exit should not be called when pings succeed")
+			default:
+			}
+		}
+
+		// No logs should be emitted during normal operation.
+		errorEntries := sink.entriesAtLevel(slog.LevelError)
+		assert.Empty(t, errorEntries,
+			"successful pings should not produce error-level logs, got: %+v", errorEntries)
+		debugEntries := sink.entriesAtLevel(slog.LevelDebug)
+		assert.Empty(t, debugEntries,
+			"successful pings should not produce debug-level logs, got: %+v", debugEntries)
+	})
+}