diff --git a/server/channels/api4/channel_bookmark_test.go b/server/channels/api4/channel_bookmark_test.go
index 1769d55020..7505240329 100644
--- a/server/channels/api4/channel_bookmark_test.go
+++ b/server/channels/api4/channel_bookmark_test.go
@@ -16,6 +16,7 @@ import (
 )
 
 func TestCreateChannelBookmark(t *testing.T) {
+	t.Skip("MM-57312")
 	os.Setenv("MM_FEATUREFLAGS_ChannelBookmarks", "true")
 	defer os.Unsetenv("MM_FEATUREFLAGS_ChannelBookmarks")
 
diff --git a/server/channels/app/plugin_db_driver.go b/server/channels/app/plugin_db_driver.go
index 56ed0ceaa2..4ab4e0c00e 100644
--- a/server/channels/app/plugin_db_driver.go
+++ b/server/channels/app/plugin_db_driver.go
@@ -12,6 +12,7 @@ import (
 
 	"github.com/mattermost/mattermost/server/public/model"
 	"github.com/mattermost/mattermost/server/public/plugin"
+	"github.com/mattermost/mattermost/server/public/shared/mlog"
 )
 
 // DriverImpl implements the plugin.Driver interface on the server-side.
@@ -21,7 +22,7 @@ import (
 type DriverImpl struct {
 	s       *Server
 	connMut sync.RWMutex
-	connMap map[string]*sql.Conn
+	connMap map[string]*connMeta
 	txMut   sync.Mutex
 	txMap   map[string]driver.Tx
 	stMut   sync.RWMutex
@@ -30,10 +31,15 @@ type DriverImpl struct {
 	rowsMap map[string]driver.Rows
 }
 
+type connMeta struct {
+	pluginID string
+	conn     *sql.Conn
+}
+
 func NewDriverImpl(s *Server) *DriverImpl {
 	return &DriverImpl{
 		s:       s,
-		connMap: make(map[string]*sql.Conn),
+		connMap: make(map[string]*connMeta),
 		txMap:   make(map[string]driver.Tx),
 		stMap:   make(map[string]driver.Stmt),
 		rowsMap: make(map[string]driver.Rows),
@@ -41,6 +47,14 @@ func NewDriverImpl(s *Server) *DriverImpl {
 }
 
 func (d *DriverImpl) Conn(isMaster bool) (string, error) {
+	return d.conn(isMaster, "")
+}
+
+func (d *DriverImpl) ConnWithPluginID(isMaster bool, pluginID string) (string, error) {
+	return d.conn(isMaster, pluginID)
+}
+
+func (d *DriverImpl) conn(isMaster bool, pluginID string) (string, error) {
 	dbFunc := d.s.Platform().Store.GetInternalMasterDB
 	if !isMaster {
 		dbFunc = d.s.Platform().Store.GetInternalReplicaDB
@@ -54,7 +68,7 @@ func (d *DriverImpl) Conn(isMaster bool) (string, error) {
 	}
 	connID := model.NewId()
 	d.connMut.Lock()
-	d.connMap[connID] = conn
+	d.connMap[connID] = &connMeta{pluginID: pluginID, conn: conn}
 	d.connMut.Unlock()
 	return connID, nil
 }
@@ -70,13 +84,13 @@ func (d *DriverImpl) Conn(isMaster bool) (string, error) {
 
 func (d *DriverImpl) ConnPing(connID string) error {
 	d.connMut.RLock()
-	conn, ok := d.connMap[connID]
+	entry, ok := d.connMap[connID]
 	d.connMut.RUnlock()
 	if !ok {
 		return driver.ErrBadConn
 	}
 
-	return conn.Raw(func(innerConn any) error {
+	return entry.conn.Raw(func(innerConn any) error {
 		return innerConn.(driver.Pinger).Ping(context.Background())
 	})
 }
@@ -84,13 +98,13 @@ func (d *DriverImpl) ConnPing(connID string) error {
 func (d *DriverImpl) ConnQuery(connID, q string, args []driver.NamedValue) (_ string, err error) {
 	var rows driver.Rows
 	d.connMut.RLock()
-	conn, ok := d.connMap[connID]
+	entry, ok := d.connMap[connID]
 	d.connMut.RUnlock()
 	if !ok {
 		return "", driver.ErrBadConn
 	}
 
-	err = conn.Raw(func(innerConn any) error {
+	err = entry.conn.Raw(func(innerConn any) error {
 		rows, err = innerConn.(driver.QueryerContext).QueryContext(context.Background(), q, args)
 		return err
 	})
@@ -110,13 +124,13 @@ func (d *DriverImpl) ConnExec(connID, q string, args []driver.NamedValue) (_ plu
 	var res driver.Result
 	var ret plugin.ResultContainer
 	d.connMut.RLock()
-	conn, ok := d.connMap[connID]
+	entry, ok := d.connMap[connID]
 	d.connMut.RUnlock()
 	if !ok {
 		return ret, driver.ErrBadConn
 	}
 
-	err = conn.Raw(func(innerConn any) error {
+	err = entry.conn.Raw(func(innerConn any) error {
 		res, err = innerConn.(driver.ExecerContext).ExecContext(context.Background(), q, args)
 		return err
 	})
@@ -132,7 +146,7 @@ func (d *DriverImpl) ConnExec(connID, q string, args []driver.NamedValue) (_ plu
 
 func (d *DriverImpl) ConnClose(connID string) error {
 	d.connMut.Lock()
-	conn, ok := d.connMap[connID]
+	entry, ok := d.connMap[connID]
 	if !ok {
 		d.connMut.Unlock()
 		return driver.ErrBadConn
@@ -140,19 +154,35 @@ func (d *DriverImpl) ConnClose(connID string) error {
 	delete(d.connMap, connID)
 	d.connMut.Unlock()
 
-	return conn.Close()
+	return entry.conn.Close()
+}
+
+// ShutdownConns will close any remaining connections for the given pluginID
+// if they weren't already closed by the plugin itself.
+func (d *DriverImpl) ShutdownConns(pluginID string) {
+	d.connMut.Lock()
+	defer d.connMut.Unlock()
+	for connID, entry := range d.connMap {
+		if entry.pluginID == pluginID {
+			err := entry.conn.Close()
+			if err != nil {
+				d.s.Log().Error("Error while closing DB connection", mlog.Err(err), mlog.String("pluginID", pluginID))
+			}
+			delete(d.connMap, connID)
+		}
+	}
 }
 
 func (d *DriverImpl) Tx(connID string, opts driver.TxOptions) (_ string, err error) {
 	var tx driver.Tx
 	d.connMut.RLock()
-	conn, ok := d.connMap[connID]
+	entry, ok := d.connMap[connID]
 	d.connMut.RUnlock()
 	if !ok {
 		return "", driver.ErrBadConn
 	}
 
-	err = conn.Raw(func(innerConn any) error {
+	err = entry.conn.Raw(func(innerConn any) error {
 		tx, err = innerConn.(driver.ConnBeginTx).BeginTx(context.Background(), opts)
 		return err
 	})
@@ -188,13 +218,13 @@ func (d *DriverImpl) TxRollback(txID string) error {
 func (d *DriverImpl) Stmt(connID, q string) (_ string, err error) {
 	var stmt driver.Stmt
 	d.connMut.RLock()
-	conn, ok := d.connMap[connID]
+	entry, ok := d.connMap[connID]
 	d.connMut.RUnlock()
 	if !ok {
 		return "", driver.ErrBadConn
 	}
 
-	err = conn.Raw(func(innerConn any) error {
+	err = entry.conn.Raw(func(innerConn any) error {
 		stmt, err = innerConn.(driver.Conn).Prepare(q)
 		return err
 	})
diff --git a/server/channels/app/plugin_db_driver_test.go b/server/channels/app/plugin_db_driver_test.go
index a2c428fb6f..6f9c8f0d61 100644
--- a/server/channels/app/plugin_db_driver_test.go
+++ b/server/channels/app/plugin_db_driver_test.go
@@ -19,3 +19,22 @@ func TestConnCreateTimeout(t *testing.T) {
 	_, err := d.Conn(true)
 	require.Error(t, err)
 }
+
+func TestShutdownPluginConns(t *testing.T) {
+	th := Setup(t)
+	defer th.TearDown()
+
+	d := NewDriverImpl(th.Server)
+	_, err := d.ConnWithPluginID(true, "plugin1")
+	require.NoError(t, err)
+	_, err = d.ConnWithPluginID(true, "plugin2")
+	require.NoError(t, err)
+	_, err = d.ConnWithPluginID(true, "plugin1")
+	require.NoError(t, err)
+
+	require.Len(t, d.connMap, 3)
+	d.ShutdownConns("plugin1")
+	require.Len(t, d.connMap, 1)
+	d.ShutdownConns("plugin2")
+	require.Len(t, d.connMap, 0)
+}
diff --git a/server/public/plugin/driver.go b/server/public/plugin/driver.go
index 68eebeea1c..ba5c5d9aca 100644
--- a/server/public/plugin/driver.go
+++ b/server/public/plugin/driver.go
@@ -62,3 +62,14 @@ type Driver interface {
 	// ResetSession(ctx context.Context) error
 	// IsValid() bool
 }
+
+// AppDriver is an extension of the Driver interface to capture non-RPC APIs.
+type AppDriver interface {
+	Driver
+
+	// ConnWithPluginID is only used by the server, and isn't exposed via the RPC API.
+	ConnWithPluginID(isMaster bool, pluginID string) (string, error)
+	// This is an extra method needed to shutdown connections
+	// after a plugin shuts down.
+	ShutdownConns(pluginID string)
+}
diff --git a/server/public/plugin/environment.go b/server/public/plugin/environment.go
index ccca0466d2..21054ad857 100644
--- a/server/public/plugin/environment.go
+++ b/server/public/plugin/environment.go
@@ -54,7 +54,7 @@ type Environment struct {
 	logger                           *mlog.Logger
 	metrics                          metricsInterface
 	newAPIImpl                       apiImplCreatorFunc
-	dbDriver                         Driver
+	dbDriver                         AppDriver
 	pluginDir                        string
 	webappPluginDir                  string
 	prepackagedPlugins               []*PrepackagedPlugin
@@ -64,7 +64,7 @@ type Environment struct {
 
 func NewEnvironment(
 	newAPIImpl apiImplCreatorFunc,
-	dbDriver Driver,
+	dbDriver AppDriver,
 	pluginDir string,
 	webappPluginDir string,
 	logger *mlog.Logger,
diff --git a/server/public/plugin/supervisor.go b/server/public/plugin/supervisor.go
index 3ab7add785..48ada556b2 100644
--- a/server/public/plugin/supervisor.go
+++ b/server/public/plugin/supervisor.go
@@ -24,6 +24,8 @@ import (
 
 type supervisor struct {
 	lock         sync.RWMutex
+	pluginID     string
+	appDriver    AppDriver
 	client       *plugin.Client
 	hooks        Hooks
 	implemented  [TotalHooksID]bool
@@ -31,6 +33,15 @@ type supervisor struct {
 	isReattached bool
 }
 
+type driverForPlugin struct {
+	AppDriver
+	pluginID string
+}
+
+func (d *driverForPlugin) Conn(isMaster bool) (string, error) {
+	return d.AppDriver.ConnWithPluginID(isMaster, d.pluginID)
+}
+
 func WithExecutableFromManifest(pluginInfo *model.BundleInfo) func(*supervisor, *plugin.ClientConfig) error {
 	return func(_ *supervisor, clientConfig *plugin.ClientConfig) error {
 		executable := pluginInfo.Manifest.GetExecutableForRuntime(runtime.GOOS, runtime.GOARCH)
@@ -74,8 +85,14 @@ func WithReattachConfig(pluginReattachConfig *model.PluginReattachConfig) func(*
 	}
 }
 
-func newSupervisor(pluginInfo *model.BundleInfo, apiImpl API, driver Driver, parentLogger *mlog.Logger, metrics metricsInterface, opts ...func(*supervisor, *plugin.ClientConfig) error) (retSupervisor *supervisor, retErr error) {
-	sup := supervisor{}
+func newSupervisor(pluginInfo *model.BundleInfo, apiImpl API, driver AppDriver, parentLogger *mlog.Logger, metrics metricsInterface, opts ...func(*supervisor, *plugin.ClientConfig) error) (retSupervisor *supervisor, retErr error) {
+	sup := supervisor{
+		pluginID: pluginInfo.Manifest.Id,
+	}
+	if driver != nil {
+		sup.appDriver = &driverForPlugin{AppDriver: driver, pluginID: pluginInfo.Manifest.Id}
+	}
+
 	defer func() {
 		if retErr != nil {
 			sup.Shutdown()
@@ -92,7 +109,7 @@ func newSupervisor(pluginInfo *model.BundleInfo, apiImpl API, driver Driver, par
 	pluginMap := map[string]plugin.Plugin{
 		"hooks": &hooksPlugin{
 			log:        wrappedLogger,
-			driverImpl: driver,
+			driverImpl: sup.appDriver,
 			apiImpl:    &apiTimerLayer{pluginInfo.Manifest.Id, apiImpl, metrics},
 		},
 	}
@@ -166,8 +183,12 @@ func (sup *supervisor) Shutdown() {
 	}
 
 	// Wait for API RPC server and DB RPC server to exit.
+	// And then shutdown conns.
 	if sup.hooksClient != nil {
 		sup.hooksClient.doneWg.Wait()
+		if sup.appDriver != nil {
+			sup.appDriver.ShutdownConns(sup.pluginID)
+		}
 	}
 }