diff --git a/internal/cmd/commands/dev/dev.go b/internal/cmd/commands/dev/dev.go
index 80a22b60ef..086586824b 100644
--- a/internal/cmd/commands/dev/dev.go
+++ b/internal/cmd/commands/dev/dev.go
@@ -618,7 +618,7 @@ func (c *Command) Run(args []string) int {
 
 		if err := c.controller.Start(); err != nil {
 			retErr := fmt.Errorf("Error starting controller: %w", err)
-			if err := c.controller.Shutdown(false); err != nil {
+			if err := c.controller.Shutdown(); err != nil {
 				c.UI.Error(retErr.Error())
 				retErr = fmt.Errorf("Error shutting down controller: %w", err)
 			}
@@ -647,7 +647,7 @@ func (c *Command) Run(args []string) int {
 				retErr = fmt.Errorf("Error shutting down worker: %w", err)
 			}
 			c.UI.Error(retErr.Error())
-			if err := c.controller.Shutdown(false); err != nil {
+			if err := c.controller.Shutdown(); err != nil {
 				c.UI.Error(fmt.Errorf("Error with controller shutdown: %w", err).Error())
 			}
 			return base.CommandCliError
@@ -684,7 +684,7 @@ func (c *Command) Run(args []string) int {
 				}
 			}
 
-			if err := c.controller.Shutdown(false); err != nil {
+			if err := c.controller.Shutdown(); err != nil {
 				c.UI.Error(fmt.Errorf("Error shutting down controller: %w", err).Error())
 			}
 
diff --git a/internal/cmd/commands/server/server.go b/internal/cmd/commands/server/server.go
index 5cc12688ee..2d5763ad0f 100644
--- a/internal/cmd/commands/server/server.go
+++ b/internal/cmd/commands/server/server.go
@@ -465,7 +465,7 @@ func (c *Command) Run(args []string) int {
 		if err := c.StartWorker(); err != nil {
 			c.UI.Error(err.Error())
 			if c.controller != nil {
-				if err := c.controller.Shutdown(false); err != nil {
+				if err := c.controller.Shutdown(); err != nil {
 					c.UI.Error(fmt.Errorf("Error with controller shutdown: %w", err).Error())
 				}
 			}
@@ -601,7 +601,7 @@ func (c *Command) StartController(ctx context.Context) error {
 
 	if err := c.controller.Start(); err != nil {
 		retErr := fmt.Errorf("Error starting controller: %w", err)
-		if err := c.controller.Shutdown(false); err != nil {
+		if err := c.controller.Shutdown(); err != nil {
 			c.UI.Error(retErr.Error())
 			retErr = fmt.Errorf("Error shutting down controller: %w", err)
 		}
@@ -669,7 +669,7 @@ func (c *Command) WaitForInterrupt() int {
 
 			// Do controller shutdown
 			if c.Config.Controller != nil {
-				if err := c.controller.Shutdown(c.Config.Worker != nil); err != nil {
+				if err := c.controller.Shutdown(); err != nil {
 					c.UI.Error(fmt.Errorf("Error shutting down controller: %w", err).Error())
 				}
 			}
diff --git a/internal/servers/controller/controller.go b/internal/servers/controller/controller.go
index 4a104da979..214d6e40db 100644
--- a/internal/servers/controller/controller.go
+++ b/internal/servers/controller/controller.go
@@ -352,15 +352,15 @@ func (c *Controller) registerSessionConnectionCleanupJob() error {
 	return nil
 }
 
-func (c *Controller) Shutdown(serversOnly bool) error {
+func (c *Controller) Shutdown() error {
 	const op = "controller.(Controller).Shutdown"
 	if !c.started.Load() {
 		event.WriteSysEvent(context.TODO(), op, "already shut down, skipping")
 	}
 	defer c.started.Store(false)
 	c.baseCancel()
-	if err := c.stopListeners(serversOnly); err != nil {
-		return fmt.Errorf("error stopping controller listeners: %w", err)
+	if err := c.stopServersAndListeners(); err != nil {
+		return fmt.Errorf("error stopping controller servers and listeners: %w", err)
 	}
 	c.schedulerWg.Wait()
 	c.tickerWg.Wait()
diff --git a/internal/servers/controller/listeners.go b/internal/servers/controller/listeners.go
index 8e5852870d..d7da78a88f 100644
--- a/internal/servers/controller/listeners.go
+++ b/internal/servers/controller/listeners.go
@@ -9,11 +9,9 @@ import (
 	"net"
 	"net/http"
 	"os"
-	"sync"
 	"time"
 
 	grpc_middleware "github.com/grpc-ecosystem/go-grpc-middleware"
-	"github.com/hashicorp/boundary/globals"
 	"github.com/hashicorp/boundary/internal/cmd/base"
 	pbs "github.com/hashicorp/boundary/internal/gen/controller/servers/services"
 	"github.com/hashicorp/boundary/internal/libs/alpnmux"
@@ -162,61 +160,108 @@ func (c *Controller) configureForCluster(ln *base.ServerListener) (func(), error
 	return func() { go ln.GrpcServer.Serve(ln.ALPNListener) }, nil
 }
 
-func (c *Controller) stopListeners(serversOnly bool) error {
-	serverWg := new(sync.WaitGroup)
-	for _, ln := range c.conf.Listeners {
-		localLn := ln
-		serverWg.Add(1)
-		go func() {
-			defer serverWg.Done()
-
-			shutdownKill, shutdownKillCancel := context.WithTimeout(c.baseContext, localLn.Config.MaxRequestDuration)
-			defer shutdownKillCancel()
-
-			if localLn.GrpcServer != nil {
-				// Deal with the worst case
-				go func() {
-					<-shutdownKill.Done()
-					localLn.GrpcServer.Stop()
-				}()
-				localLn.GrpcServer.GracefulStop()
-			}
-			if localLn.HTTPServer != nil {
-				localLn.HTTPServer.Shutdown(shutdownKill)
-			}
-		}()
+func (c *Controller) stopServersAndListeners() error {
+	var mg multierror.Group
+	mg.Go(c.stopClusterGrpcServerAndListener)
+	mg.Go(c.stopHttpServersAndListeners)
+	mg.Go(c.stopApiGrpcServerAndListener)
+
+	stopErrors := mg.Wait()
+
+	err := c.stopAnyListeners()
+	if err != nil {
+		stopErrors = multierror.Append(stopErrors, err)
+	}
+
+	return stopErrors.ErrorOrNil()
+}
+
+func (c *Controller) stopClusterGrpcServerAndListener() error {
+	if c.clusterListener == nil {
+		return nil
 	}
+	if c.clusterListener.GrpcServer == nil {
+		return fmt.Errorf("no cluster grpc server")
+	}
+	if c.clusterListener.Mux == nil {
+		return fmt.Errorf("no cluster listener mux")
+	}
+
+	c.clusterListener.GrpcServer.GracefulStop()
+	err := c.clusterListener.Mux.Close()
+	return listenerCloseErrorCheck(c.clusterListener.Config.Type, err)
+}
+
+func (c *Controller) stopHttpServersAndListeners() error {
+	var closeErrors *multierror.Error
+	for i := range c.apiListeners {
+		ln := c.apiListeners[i]
+		if ln.HTTPServer == nil {
+			continue
+		}
 
-	if c.apiGrpcServer != nil {
-		serverWg.Add(1)
-		go func() {
-			defer serverWg.Done()
-			shutdownKill, shutdownKillCancel := context.WithTimeout(c.baseContext, globals.DefaultMaxRequestDuration)
-			defer shutdownKillCancel()
-			go func() {
-				<-shutdownKill.Done()
-				c.apiGrpcServer.Stop()
-			}()
-			c.apiGrpcServer.GracefulStop()
-		}()
+		ctx, cancel := context.WithTimeout(c.baseContext, ln.Config.MaxRequestDuration)
+		ln.HTTPServer.Shutdown(ctx)
+		cancel()
+
+		err := ln.Mux.Close() // The HTTP Shutdown call should close this, but just in case.
+		err = listenerCloseErrorCheck(ln.Config.Type, err)
+		if err != nil {
+			multierror.Append(closeErrors, err)
+		}
 	}
 
-	serverWg.Wait()
-	if serversOnly {
+	return closeErrors.ErrorOrNil()
+}
+
+func (c *Controller) stopApiGrpcServerAndListener() error {
+	if c.apiGrpcServer == nil {
 		return nil
 	}
-	var retErr *multierror.Error
-	for _, ln := range c.conf.Listeners {
-		if err := ln.Mux.Close(); err != nil {
-			if _, ok := err.(*os.PathError); ok && ln.Config.Type == "unix" {
-				// The rmListener probably tried to remove the file but it
-				// didn't exist, ignore the error; this is a conflict
-				// between rmListener and the default Go behavior of
-				// removing auto-vivified Unix domain sockets.
-			} else {
-				retErr = multierror.Append(retErr, err)
-			}
+
+	c.apiGrpcServer.GracefulStop()
+	err := c.apiGrpcServerListener.Close()
+	return listenerCloseErrorCheck("ch", err) // apiGrpcServerListener is just a channel, so the type here is not important.
+}
+
+// stopAnyListeners does a final once over the known
+// listeners to make sure we didn't miss any;
+// expected to run at the end of stopServersAndListeners.
+func (c *Controller) stopAnyListeners() error {
+	var closeErrors *multierror.Error
+	for i := range c.apiListeners {
+		ln := c.apiListeners[i]
+		if ln == nil || ln.Mux == nil {
+			continue
+		}
+
+		err := ln.Mux.Close()
+		err = listenerCloseErrorCheck(ln.Config.Type, err)
+		if err != nil {
+			multierror.Append(closeErrors, err)
 		}
 	}
-	return retErr.ErrorOrNil()
+
+	return closeErrors.ErrorOrNil()
+}
+
+// listenerCloseErrorCheck does some validation on an error returned
+// by a net.Listener's Close function, and ignores a few cases
+// where we don't actually want an error to be returned.
+func listenerCloseErrorCheck(lnType string, err error) error {
+	if errors.Is(err, net.ErrClosed) {
+		// Ignore net.ErrClosed - The listener was already closed,
+		// so there's nothing else to do.
+		return nil
+	}
+	if _, ok := err.(*os.PathError); ok && lnType == "unix" {
+		// The underlying rmListener probably tried to remove
+		// the file but it didn't exist, ignore the error;
+		// this is a conflict between rmListener and the
+		// default Go behavior of removing auto-vivified
+		// Unix domain sockets.
+		return nil
+	}
+
+	return err
 }
diff --git a/internal/servers/controller/listeners_test.go b/internal/servers/controller/listeners_test.go
index e674882b86..daf0135a01 100644
--- a/internal/servers/controller/listeners_test.go
+++ b/internal/servers/controller/listeners_test.go
@@ -20,6 +20,7 @@ import (
 	"time"
 
 	"github.com/hashicorp/boundary/internal/cmd/base"
+	"github.com/hashicorp/boundary/internal/libs/alpnmux"
 	"github.com/hashicorp/go-secure-stdlib/base62"
 	"github.com/hashicorp/go-secure-stdlib/configutil/v2"
 	"github.com/hashicorp/go-secure-stdlib/listenerutil"
@@ -262,6 +263,454 @@ func TestStartListeners(t *testing.T) {
 	}
 }
 
+func TestStopClusterGrpcServerAndListener(t *testing.T) {
+	tests := []struct {
+		name         string
+		controllerFn func(t *testing.T) *Controller
+		assertions   func(t *testing.T, c *Controller)
+		expErr       bool
+		expErrStr    string
+	}{
+		{
+			name: "no cluster listener",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{}
+			},
+			expErr: false,
+		},
+		{
+			name: "no cluster grpc server",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{clusterListener: &base.ServerListener{}}
+			},
+			expErr:    true,
+			expErrStr: "no cluster grpc server",
+		},
+		{
+			name: "no cluster listener mux",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{
+					clusterListener: &base.ServerListener{
+						GrpcServer: grpc.NewServer(),
+						Config:     &listenerutil.ListenerConfig{Type: "tcp"},
+					},
+				}
+			},
+			expErr:    true,
+			expErrStr: "no cluster listener mux",
+		},
+		{
+			name: "listener already closed",
+			controllerFn: func(t *testing.T) *Controller {
+				l, err := net.Listen("tcp", "127.0.0.1:0")
+				require.NoError(t, err)
+				require.NoError(t, l.Close())
+
+				return &Controller{
+					clusterListener: &base.ServerListener{
+						ALPNListener: l,
+						GrpcServer:   grpc.NewServer(),
+						Mux:          alpnmux.New(l),
+						Config:       &listenerutil.ListenerConfig{Type: "tcp"},
+					},
+				}
+			},
+			assertions: func(t *testing.T, c *Controller) {
+				require.ErrorIs(t, c.clusterListener.Mux.Close(), net.ErrClosed)
+			},
+			expErr: false,
+		},
+		{
+			name: "graceful stop",
+			controllerFn: func(t *testing.T) *Controller {
+				l, err := net.Listen("tcp", "127.0.0.1:0")
+				require.NoError(t, err)
+
+				grpcServer := grpc.NewServer()
+				go grpcServer.Serve(l)
+
+				// Make sure it's up
+				_, err = grpc.Dial(l.Addr().String(),
+					grpc.WithInsecure(),
+					grpc.WithBlock(),
+					grpc.WithTimeout(5*time.Second),
+				)
+				require.NoError(t, err)
+
+				return &Controller{
+					clusterListener: &base.ServerListener{
+						ALPNListener: l,
+						GrpcServer:   grpcServer,
+						Mux:          alpnmux.New(l),
+						Config:       &listenerutil.ListenerConfig{Type: "tcp"},
+					},
+				}
+			},
+			assertions: func(t *testing.T, c *Controller) {
+				require.ErrorIs(t, c.clusterListener.Mux.Close(), net.ErrClosed)
+			},
+			expErr: false,
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			c := tt.controllerFn(t)
+			err := c.stopClusterGrpcServerAndListener()
+			if tt.expErr {
+				require.EqualError(t, err, tt.expErrStr)
+				return
+			}
+
+			require.NoError(t, err)
+			if tt.assertions != nil {
+				tt.assertions(t, c)
+			}
+		})
+	}
+}
+
+func TestStopHttpServersAndListeners(t *testing.T) {
+	tests := []struct {
+		name         string
+		controllerFn func(t *testing.T) *Controller
+		assertions   func(t *testing.T, c *Controller)
+		expErr       bool
+		expErrStr    string
+	}{
+		{
+			name: "no listeners",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{
+					apiListeners: []*base.ServerListener{},
+				}
+			},
+			expErr: false,
+		},
+		{
+			name: "nil listeners",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{
+					apiListeners: nil,
+				}
+			},
+			expErr: false,
+		},
+		{
+			name: "listeners with nil http server",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{
+					apiListeners: []*base.ServerListener{
+						{HTTPServer: nil},
+						{HTTPServer: nil},
+						{HTTPServer: nil},
+					},
+				}
+			},
+			expErr: false,
+		},
+		{
+			name: "listener already closed",
+			controllerFn: func(t *testing.T) *Controller {
+				l1, err := net.Listen("tcp", "127.0.0.1:0")
+				require.NoError(t, err)
+				require.NoError(t, l1.Close())
+
+				s1 := &http.Server{}
+				return &Controller{
+					baseContext: context.Background(),
+					apiListeners: []*base.ServerListener{
+						{
+							ALPNListener: l1,
+							HTTPServer:   s1,
+							Mux:          alpnmux.New(l1),
+							Config:       &listenerutil.ListenerConfig{Type: "tcp"},
+						},
+					},
+				}
+			},
+			assertions: func(t *testing.T, c *Controller) {
+				// Asserts the HTTP Servers are closed.
+				require.ErrorIs(t, c.apiListeners[0].HTTPServer.Serve(c.apiListeners[0].ALPNListener), http.ErrServerClosed)
+
+				// Asserts the underlying listeners are closed.
+				require.ErrorIs(t, c.apiListeners[0].Mux.Close(), net.ErrClosed)
+			},
+			expErr: false,
+		},
+		{
+			name: "multiple listeners",
+			controllerFn: func(t *testing.T) *Controller {
+				l1, err := net.Listen("tcp", "127.0.0.1:0")
+				require.NoError(t, err)
+				l2, err := net.Listen("unix", "/tmp/boundary-controller-TestStopHttpServersAndListeners-"+strconv.FormatInt(time.Now().UnixNano(), 10))
+				require.NoError(t, err)
+
+				s1 := &http.Server{}
+				s2 := &http.Server{}
+
+				go s1.Serve(l1)
+				go s2.Serve(l2)
+
+				// Make sure they're up
+				_, err = http.Get("http://" + l1.Addr().String())
+				require.NoError(t, err)
+
+				c := http.Client{Transport: &http.Transport{
+					Dial: func(network, addr string) (net.Conn, error) {
+						return net.Dial("unix", l2.Addr().String())
+					},
+				}}
+				_, err = c.Get("http://random.domain")
+				require.NoError(t, err)
+
+				return &Controller{
+					baseContext: context.Background(),
+					apiListeners: []*base.ServerListener{
+						{
+							ALPNListener: l1,
+							HTTPServer:   s1,
+							Mux:          alpnmux.New(l1),
+							Config:       &listenerutil.ListenerConfig{Type: "tcp"},
+						},
+						{
+							ALPNListener: l2,
+							HTTPServer:   s2,
+							Mux:          alpnmux.New(l2),
+							Config:       &listenerutil.ListenerConfig{Type: "tcp"},
+						},
+					},
+				}
+			},
+			assertions: func(t *testing.T, c *Controller) {
+				// Asserts the HTTP Servers are closed.
+				require.ErrorIs(t, c.apiListeners[0].HTTPServer.Serve(c.apiListeners[0].ALPNListener), http.ErrServerClosed)
+				require.ErrorIs(t, c.apiListeners[1].HTTPServer.Serve(c.apiListeners[1].ALPNListener), http.ErrServerClosed)
+
+				// Asserts the underlying listeners are closed.
+				require.ErrorIs(t, c.apiListeners[0].Mux.Close(), net.ErrClosed)
+				require.ErrorIs(t, c.apiListeners[1].Mux.Close(), net.ErrClosed)
+			},
+			expErr: false,
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			c := tt.controllerFn(t)
+			err := c.stopHttpServersAndListeners()
+			if tt.expErr {
+				require.EqualError(t, err, tt.expErrStr)
+				return
+			}
+
+			require.NoError(t, err)
+			if tt.assertions != nil {
+				tt.assertions(t, c)
+			}
+		})
+	}
+}
+
+func TestStopApiGrpcServerAndListener(t *testing.T) {
+	tests := []struct {
+		name         string
+		controllerFn func(t *testing.T) *Controller
+		assertions   func(t *testing.T, c *Controller)
+		expErr       bool
+		expErrStr    string
+	}{
+		{
+			name: "nil api grpc server",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{apiGrpcServer: nil}
+			},
+			expErr: false,
+		},
+		{
+			name: "graceful stop",
+			controllerFn: func(t *testing.T) *Controller {
+				l := newGrpcServerListener()
+				grpcServer := grpc.NewServer()
+
+				go grpcServer.Serve(l)
+
+				// Make sure it's up
+				_, err := grpc.Dial("",
+					grpc.WithInsecure(),
+					grpc.WithBlock(),
+					grpc.WithTimeout(10*time.Second),
+					grpc.WithDialer(func(s string, d time.Duration) (net.Conn, error) {
+						return l.Dial()
+					}),
+				)
+				require.NoError(t, err)
+				return &Controller{apiGrpcServer: grpcServer, apiGrpcServerListener: l}
+			},
+			assertions: func(t *testing.T, c *Controller) {
+				require.ErrorIs(t, c.apiGrpcServer.Serve(c.apiGrpcServerListener), grpc.ErrServerStopped)
+			},
+			expErr: false,
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			c := tt.controllerFn(t)
+			err := c.stopApiGrpcServerAndListener()
+			if tt.expErr {
+				require.EqualError(t, err, tt.expErrStr)
+				return
+			}
+
+			require.NoError(t, err)
+			if tt.assertions != nil {
+				tt.assertions(t, c)
+			}
+		})
+	}
+}
+
+func TestStopAnyListeners(t *testing.T) {
+	tests := []struct {
+		name         string
+		controllerFn func(t *testing.T) *Controller
+		assertions   func(t *testing.T, c *Controller)
+		expErr       bool
+		expErrStr    string
+	}{
+		{
+			name: "nil apiListeners",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{apiListeners: nil}
+			},
+			expErr: false,
+		},
+		{
+			name: "no listeners",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{apiListeners: []*base.ServerListener{}}
+			},
+			expErr: false,
+		},
+		{
+			name: "nil listeners",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{apiListeners: []*base.ServerListener{nil, nil, nil}}
+			},
+			expErr: false,
+		},
+		{
+			name: "listeners with nil mux",
+			controllerFn: func(t *testing.T) *Controller {
+				return &Controller{apiListeners: []*base.ServerListener{
+					{Mux: nil}, {Mux: nil}, {Mux: nil},
+				}}
+			},
+			expErr: false,
+		},
+		{
+			name: "multiple listeners, including a closed one",
+			controllerFn: func(t *testing.T) *Controller {
+				l1, err := net.Listen("tcp", "127.0.0.1:0")
+				require.NoError(t, err)
+
+				l2, err := net.Listen("unix", "/tmp/boundary-controller-TestStopAnyListeners-"+strconv.FormatInt(time.Now().UnixNano(), 10))
+				require.NoError(t, err)
+
+				l3, err := net.Listen("tcp", "127.0.0.1:0")
+				require.NoError(t, err)
+				require.NoError(t, l3.Close())
+
+				return &Controller{apiListeners: []*base.ServerListener{
+					{
+						Config: &listenerutil.ListenerConfig{Type: "tcp"},
+						Mux:    alpnmux.New(l1),
+					},
+					{
+						Config: &listenerutil.ListenerConfig{Type: "tcp"},
+						Mux:    alpnmux.New(l2),
+					},
+					{
+						Config: &listenerutil.ListenerConfig{Type: "tcp"},
+						Mux:    alpnmux.New(l3),
+					},
+				}}
+			},
+			assertions: func(t *testing.T, c *Controller) {
+				for i := range c.apiListeners {
+					ln := c.apiListeners[i]
+					require.ErrorIs(t, ln.Mux.Close(), net.ErrClosed)
+				}
+			},
+			expErr: false,
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			c := tt.controllerFn(t)
+			err := c.stopAnyListeners()
+			if tt.expErr {
+				require.EqualError(t, err, tt.expErrStr)
+				return
+			}
+
+			require.NoError(t, err)
+			if tt.assertions != nil {
+				tt.assertions(t, c)
+			}
+		})
+	}
+}
+
+func TestListenerCloseErrorCheck(t *testing.T) {
+	tests := []struct {
+		name   string
+		lnType string
+		err    error
+		expErr error
+	}{
+		{
+			name:   "nil err",
+			lnType: "tcp",
+			err:    nil,
+			expErr: nil,
+		},
+		{
+			name:   "net.Closed",
+			lnType: "tcp",
+			err:    net.ErrClosed,
+			expErr: nil,
+		},
+		{
+			name:   "path err not unix type",
+			lnType: "tcp",
+			err:    &os.PathError{Op: "test"},
+			expErr: &os.PathError{Op: "test"},
+		},
+		{
+			name:   "path err unix type",
+			lnType: "unix",
+			err:    &os.PathError{Op: "test"},
+			expErr: nil,
+		},
+		{
+			name:   "literally anything else",
+			lnType: "tcp",
+			err:    fmt.Errorf("oops I errored"),
+			expErr: fmt.Errorf("oops I errored"),
+		},
+	}
+
+	for _, tt := range tests {
+		t.Run(tt.name, func(t *testing.T) {
+			err := listenerCloseErrorCheck(tt.lnType, tt.err)
+			require.Equal(t, tt.expErr, err)
+		})
+	}
+}
+
 func clusterGrpcDialNoError(t *testing.T, c *Controller, network, addr string) {
 	grpcConn, err := grpc.Dial(addr,
 		grpc.WithInsecure(),
diff --git a/internal/servers/controller/testing.go b/internal/servers/controller/testing.go
index 7648d3d85d..d6e34af983 100644
--- a/internal/servers/controller/testing.go
+++ b/internal/servers/controller/testing.go
@@ -279,7 +279,7 @@ func (tc *TestController) Shutdown() {
 	tc.cancel()
 
 	if tc.c != nil {
-		if err := tc.c.Shutdown(false); err != nil {
+		if err := tc.c.Shutdown(); err != nil {
 			tc.t.Error(err)
 		}
 	}
diff --git a/internal/tests/cluster/ipv6_listener_test.go b/internal/tests/cluster/ipv6_listener_test.go
index 421c37baeb..4f60f2bed7 100644
--- a/internal/tests/cluster/ipv6_listener_test.go
+++ b/internal/tests/cluster/ipv6_listener_test.go
@@ -77,16 +77,18 @@ func TestIPv6Listener(t *testing.T) {
 	time.Sleep(10 * time.Second)
 	expectWorkers(c1, w1)
 
-	require.NoError(w1.Worker().Shutdown(true))
-	time.Sleep(10 * time.Second)
-	expectWorkers(c1)
+	c2 := c1.AddClusterControllerMember(t, &controller.TestControllerOpts{
+		Logger: c1.Config().Logger.ResetNamed("c2"),
+	})
+	defer c2.Shutdown()
 
-	require.NoError(c1.Controller().Shutdown(true))
 	time.Sleep(10 * time.Second)
+	expectWorkers(c2, w1)
 
-	require.NoError(c1.Controller().Start())
+	require.NoError(w1.Worker().Shutdown(true))
 	time.Sleep(10 * time.Second)
-	expectWorkers(c1, w1)
+	expectWorkers(c1)
+	expectWorkers(c2)
 
 	client, err := api.NewClient(nil)
 	require.NoError(err)
diff --git a/internal/tests/cluster/multi_controller_worker_test.go b/internal/tests/cluster/multi_controller_worker_test.go
index 272e5a0b40..cb39bb6304 100644
--- a/internal/tests/cluster/multi_controller_worker_test.go
+++ b/internal/tests/cluster/multi_controller_worker_test.go
@@ -64,7 +64,7 @@ func TestMultiControllerMultiWorkerConnections(t *testing.T) {
 	expectWorkers(t, c1, w1, w2)
 	expectWorkers(t, c2, w1, w2)
 
-	require.NoError(c1.Controller().Shutdown(true))
+	require.NoError(c2.Controller().Shutdown())
 	time.Sleep(10 * time.Second)
 	expectWorkers(t, c2, w1, w2)
 
diff --git a/internal/tests/cluster/unix_listener_test.go b/internal/tests/cluster/unix_listener_test.go
index d3e5473ce2..c7248a6e99 100644
--- a/internal/tests/cluster/unix_listener_test.go
+++ b/internal/tests/cluster/unix_listener_test.go
@@ -94,12 +94,16 @@ func TestUnixListener(t *testing.T) {
 	time.Sleep(10 * time.Second)
 	expectWorkers(c1)
 
-	require.NoError(c1.Controller().Shutdown(true))
-	time.Sleep(10 * time.Second)
+	require.NoError(c1.Controller().Shutdown())
+	c1 = controller.NewTestController(t, &controller.TestControllerOpts{
+		Config:                        conf,
+		Logger:                        logger.Named("c1"),
+		DisableOidcAuthMethodCreation: true,
+	})
+	defer c1.Shutdown()
 
-	require.NoError(c1.Controller().Start())
 	time.Sleep(10 * time.Second)
-	expectWorkers(c1, w1)
+	expectWorkers(c1)
 
 	client, err := api.NewClient(nil)
 	require.NoError(err)