diff --git a/tsdb/db.go b/tsdb/db.go
index ff1d6876d6..0e92c2b70e 100644
--- a/tsdb/db.go
+++ b/tsdb/db.go
@@ -1277,7 +1277,7 @@ func (db *DB) ApplyConfig(conf *config.Config) error {
 		// Update retention configuration if provided.
 		if conf.StorageConfig.TSDBConfig.Retention != nil {
 			db.retentionMtx.Lock()
-			db.opts.RetentionDuration = int64(conf.StorageConfig.TSDBConfig.Retention.Time)
+			db.opts.RetentionDuration = int64(time.Duration(conf.StorageConfig.TSDBConfig.Retention.Time) / time.Millisecond)
 			db.metrics.retentionDuration.Set((time.Duration(db.opts.RetentionDuration) * time.Millisecond).Seconds())
 			db.opts.MaxBytes = int64(conf.StorageConfig.TSDBConfig.Retention.Size)
 			db.metrics.maxBytes.Set(float64(db.opts.MaxBytes))
diff --git a/tsdb/db_test.go b/tsdb/db_test.go
index bd868d945a..be914cd87d 100644
--- a/tsdb/db_test.go
+++ b/tsdb/db_test.go
@@ -1743,7 +1743,7 @@ func TestRuntimeRetentionConfigChange(t *testing.T) {
 		StorageConfig: config.StorageConfig{
 			TSDBConfig: &config.TSDBConfig{
 				Retention: &config.TSDBRetentionConfig{
-					Time: model.Duration(shorterRetentionDuration),
+					Time: model.Duration(time.Duration(shorterRetentionDuration) * time.Millisecond),
 				},
 			},
 		},
@@ -1772,6 +1772,31 @@ func TestRuntimeRetentionConfigChange(t *testing.T) {
 	require.Positive(t, int(prom_testutil.ToFloat64(db.metrics.timeRetentionCount)), "time retention count should be incremented")
 }
 
+// TestApplyConfigRetentionDurationMetricUnit verifies that after a config
+// reload the prometheus_tsdb_retention_limit_seconds metric reports the
+// retention in seconds.
+func TestApplyConfigRetentionDurationMetricUnit(t *testing.T) {
+	oneHourMs := int64(time.Hour / time.Millisecond)
+	db := newTestDB(t, withOpts(&Options{RetentionDuration: oneHourMs}))
+
+	cfg := &config.Config{
+		StorageConfig: config.StorageConfig{
+			TSDBConfig: &config.TSDBConfig{
+				Retention: &config.TSDBRetentionConfig{
+					Time: model.Duration(time.Hour),
+				},
+			},
+		},
+	}
+	require.NoError(t, db.ApplyConfig(cfg))
+
+	require.Equal(t, oneHourMs, db.getRetentionDuration())
+
+	gotSeconds := prom_testutil.ToFloat64(db.metrics.retentionDuration)
+	wantSeconds := time.Hour.Seconds()
+	require.Equal(t, wantSeconds, gotSeconds)
+}
+
 func TestNotMatcherSelectsLabelsUnsetSeries(t *testing.T) {
 	db := newTestDB(t)