diff --git a/api/cli/cli.go b/api/cli/cli.go
index 267f584d9..b4c0d6e10 100644
--- a/api/cli/cli.go
+++ b/api/cli/cli.go
@@ -56,6 +56,7 @@ func CLIFlags() *portainer.CLIFlags {
 		PullLimitCheckDisabled:    kingpin.Flag("pull-limit-check-disabled", "Pull limit check").Envar(portainer.PullLimitCheckDisabledEnvVar).Default(defaultPullLimitCheckDisabled).Bool(),
 		TrustedOrigins:            kingpin.Flag("trusted-origins", "List of trusted origins for CSRF protection. Separate multiple origins with a comma.").Envar(portainer.TrustedOriginsEnvVar).String(),
 		CSP:                       kingpin.Flag("csp", "Content Security Policy (CSP) header").Envar(portainer.CSPEnvVar).Default("true").Bool(),
+		CompactDB:                 kingpin.Flag("compact-db", "Enable database compaction on startup").Envar(portainer.CompactDBEnvVar).Default("false").Bool(),
 	}
 }
 
diff --git a/api/cmd/portainer/main.go b/api/cmd/portainer/main.go
index c569d0d67..691490eea 100644
--- a/api/cmd/portainer/main.go
+++ b/api/cmd/portainer/main.go
@@ -84,7 +84,7 @@ func initFileService(dataStorePath string) portainer.FileService {
 }
 
 func initDataStore(flags *portainer.CLIFlags, secretKey []byte, fileService portainer.FileService, shutdownCtx context.Context) dataservices.DataStore {
-	connection, err := database.NewDatabase("boltdb", *flags.Data, secretKey)
+	connection, err := database.NewDatabase("boltdb", *flags.Data, secretKey, *flags.CompactDB)
 	if err != nil {
 		log.Fatal().Err(err).Msg("failed creating database connection")
 	}
diff --git a/api/database/boltdb/db.go b/api/database/boltdb/db.go
index 32a1b55c3..3ff8f19d6 100644
--- a/api/database/boltdb/db.go
+++ b/api/database/boltdb/db.go
@@ -21,6 +21,9 @@ import (
 const (
 	DatabaseFileName          = "portainer.db"
 	EncryptedDatabaseFileName = "portainer.edb"
+
+	txMaxSize       = 65536
+	compactedSuffix = ".compacted"
 )
 
 var (
@@ -35,6 +38,7 @@ type DbConnection struct {
 	InitialMmapSize int
 	EncryptionKey   []byte
 	isEncrypted     bool
+	Compact         bool
 
 	*bolt.DB
 }
@@ -135,12 +139,7 @@ func (connection *DbConnection) Open() error {
 	// Now we open the db
 	databasePath := connection.GetDatabaseFilePath()
 
-	db, err := bolt.Open(databasePath, 0600, &bolt.Options{
-		Timeout:         1 * time.Second,
-		InitialMmapSize: connection.InitialMmapSize,
-		FreelistType:    bolt.FreelistMapType,
-		NoFreelistSync:  true,
-	})
+	db, err := bolt.Open(databasePath, 0600, connection.boltOptions())
 	if err != nil {
 		return err
 	}
@@ -149,6 +148,15 @@ func (connection *DbConnection) Open() error {
 	db.MaxBatchDelay = connection.MaxBatchDelay
 	connection.DB = db
 
+	if connection.Compact {
+		log.Info().Msg("compacting database")
+		if err := connection.compact(); err != nil {
+			log.Error().Err(err).Msg("failed to compact database")
+		} else {
+			log.Info().Msg("database compaction completed")
+		}
+	}
+
 	return nil
 }
 
@@ -414,3 +422,42 @@ func (connection *DbConnection) RestoreMetadata(s map[string]any) error {
 
 	return err
 }
+
+// compact attempts to compact the database and replace it iff it succeeds
+func (connection *DbConnection) compact() error {
+	compactedPath := connection.GetDatabaseFilePath() + compactedSuffix
+	compactedDB, err := bolt.Open(compactedPath, 0o600, connection.boltOptions())
+	if err != nil {
+		return fmt.Errorf("failure to create the compacted database: %w", err)
+	}
+
+	compactedDB.MaxBatchSize = connection.MaxBatchSize
+	compactedDB.MaxBatchDelay = connection.MaxBatchDelay
+
+	if err := bolt.Compact(compactedDB, connection.DB, txMaxSize); err != nil {
+		return fmt.Errorf("failure to compact the database: %w",
+			errors.Join(err, compactedDB.Close(), os.Remove(compactedPath)))
+	}
+
+	if err := os.Rename(compactedPath, connection.GetDatabaseFilePath()); err != nil {
+		return fmt.Errorf("failure to move the compacted database: %w",
+			errors.Join(err, compactedDB.Close(), os.Remove(compactedPath)))
+	}
+
+	if err := connection.Close(); err != nil {
+		log.Warn().Err(err).Msg("failure to close the database after compaction")
+	}
+
+	connection.DB = compactedDB
+
+	return nil
+}
+
+func (connection *DbConnection) boltOptions() *bolt.Options {
+	return &bolt.Options{
+		Timeout:         1 * time.Second,
+		InitialMmapSize: connection.InitialMmapSize,
+		FreelistType:    bolt.FreelistMapType,
+		NoFreelistSync:  true,
+	}
+}
diff --git a/api/database/boltdb/db_test.go b/api/database/boltdb/db_test.go
index 6e4639c68..1aba08fb8 100644
--- a/api/database/boltdb/db_test.go
+++ b/api/database/boltdb/db_test.go
@@ -6,6 +6,8 @@ import (
 	"testing"
 
 	"github.com/stretchr/testify/assert"
+	"github.com/stretchr/testify/require"
+	"go.etcd.io/bbolt"
 )
 
 func Test_NeedsEncryptionMigration(t *testing.T) {
@@ -119,3 +121,57 @@ func Test_NeedsEncryptionMigration(t *testing.T) {
 		})
 	}
 }
+
+func TestDBCompaction(t *testing.T) {
+	db := &DbConnection{
+		Path:    t.TempDir(),
+		Compact: true,
+	}
+
+	err := db.Open()
+	require.NoError(t, err)
+
+	err = db.Update(func(tx *bbolt.Tx) error {
+		b, err := tx.CreateBucketIfNotExists([]byte("testbucket"))
+		if err != nil {
+			return err
+		}
+
+		b.Put([]byte("key"), []byte("value"))
+
+		return nil
+	})
+	require.NoError(t, err)
+
+	err = db.Close()
+	require.NoError(t, err)
+
+	// Reopen the DB to trigger compaction
+	err = db.Open()
+	require.NoError(t, err)
+
+	// Check that the data is still there
+	err = db.View(func(tx *bbolt.Tx) error {
+		b := tx.Bucket([]byte("testbucket"))
+		if b == nil {
+			return nil
+		}
+
+		val := b.Get([]byte("key"))
+		require.Equal(t, []byte("value"), val)
+
+		return nil
+	})
+	require.NoError(t, err)
+
+	err = db.Close()
+	require.NoError(t, err)
+
+	// Failures
+
+	err = os.Mkdir(db.GetDatabaseFilePath()+compactedSuffix, 0o755)
+	require.NoError(t, err)
+
+	err = db.Open()
+	require.NoError(t, err)
+}
diff --git a/api/database/database.go b/api/database/database.go
index 492d56bcf..c3c3cc267 100644
--- a/api/database/database.go
+++ b/api/database/database.go
@@ -8,11 +8,12 @@ import (
 )
 
 // NewDatabase should use config options to return a connection to the requested database
-func NewDatabase(storeType, storePath string, encryptionKey []byte) (connection portainer.Connection, err error) {
+func NewDatabase(storeType, storePath string, encryptionKey []byte, compact bool) (connection portainer.Connection, err error) {
 	if storeType == "boltdb" {
 		return &boltdb.DbConnection{
 			Path:          storePath,
 			EncryptionKey: encryptionKey,
+			Compact:       compact,
 		}, nil
 	}
 
diff --git a/api/datastore/teststore.go b/api/datastore/teststore.go
index 0945195b0..5d9573a61 100644
--- a/api/datastore/teststore.go
+++ b/api/datastore/teststore.go
@@ -44,7 +44,7 @@ func NewTestStore(t testing.TB, init, secure bool) (bool, *Store, func(), error)
 		secretKey = nil
 	}
 
-	connection, err := database.NewDatabase("boltdb", storePath, secretKey)
+	connection, err := database.NewDatabase("boltdb", storePath, secretKey, false)
 	if err != nil {
 		panic(err)
 	}
diff --git a/api/internal/testhelpers/datastore.go b/api/internal/testhelpers/datastore.go
index d89b07531..0dc543cf9 100644
--- a/api/internal/testhelpers/datastore.go
+++ b/api/internal/testhelpers/datastore.go
@@ -113,7 +113,7 @@ type datastoreOption = func(d *testDatastore)
 // NewDatastore creates new instance of testDatastore.
 // Will apply options before returning, opts will be applied from left to right.
 func NewDatastore(options ...datastoreOption) *testDatastore {
-	conn, _ := database.NewDatabase("boltdb", "", nil)
+	conn, _ := database.NewDatabase("boltdb", "", nil, false)
 	d := testDatastore{connection: conn}
 
 	for _, o := range options {
diff --git a/api/portainer.go b/api/portainer.go
index c190465c9..f79ec976c 100644
--- a/api/portainer.go
+++ b/api/portainer.go
@@ -112,6 +112,7 @@ type (
 		AdminPasswordFile         *string
 		Assets                    *string
 		CSP                       *bool
+		CompactDB                 *bool
 		Data                      *string
 		FeatureFlags              *[]string
 		EnableEdgeComputeFeatures *bool
@@ -1846,6 +1847,8 @@ const (
 	TrustedOriginsEnvVar = "TRUSTED_ORIGINS"
 	// CSPEnvVar is the environment variable used to enable/disable the Content Security Policy
 	CSPEnvVar = "CSP"
+	// CompactDBEnvVar is the environment variable used to enable/disable the startup compaction of the database
+	CompactDBEnvVar = "COMPACT_DB"
 )
 
 // List of supported features