diff --git a/bootstrap/kubeadm/main.go b/bootstrap/kubeadm/main.go
index fca4f1870cce..3fd52bb94df3 100644
--- a/bootstrap/kubeadm/main.go
+++ b/bootstrap/kubeadm/main.go
@@ -71,7 +71,7 @@ var (
 	leaderElectionRenewDeadline time.Duration
 	leaderElectionRetryPeriod   time.Duration
 	watchFilterValue            string
-	watchNamespace              string
+	watchNamespacesList         []string
 	profilerAddress             string
 	enableContentionProfiling   bool
 	syncPeriod                  time.Duration
@@ -118,8 +118,8 @@ func InitFlags(fs *pflag.FlagSet) {
 	fs.DurationVar(&leaderElectionRetryPeriod, "leader-elect-retry-period", 2*time.Second,
 		"Duration the LeaderElector clients should wait between tries of actions (duration string)")
 
-	fs.StringVar(&watchNamespace, "namespace", "",
-		"Namespace that the controller watches to reconcile cluster-api objects. If unspecified, the controller watches for cluster-api objects across all namespaces.")
+	fs.StringSliceVar(&watchNamespacesList, "namespace", nil,
+		"Comma-separated list of namespaces that the controller watches to reconcile cluster-api objects. If unspecified, the controller watches for cluster-api objects across all namespaces.")
 
 	fs.StringVar(&watchFilterValue, "watch-filter", "",
 		fmt.Sprintf("Label value that the controller watches to reconcile cluster-api objects. Label key is always %s. If unspecified, the controller watches for all cluster-api objects.", clusterv1.WatchLabel))
@@ -214,9 +214,10 @@ func main() {
 	}
 
 	var watchNamespaces map[string]cache.Config
-	if watchNamespace != "" {
-		watchNamespaces = map[string]cache.Config{
-			watchNamespace: {},
+	if watchNamespacesList != nil {
+		watchNamespaces = map[string]cache.Config{}
+		for _, watchNamespace := range watchNamespacesList {
+			watchNamespaces[watchNamespace] = cache.Config{}
 		}
 	}
 
diff --git a/controlplane/kubeadm/main.go b/controlplane/kubeadm/main.go
index 3d624099fd82..d1cb39618521 100644
--- a/controlplane/kubeadm/main.go
+++ b/controlplane/kubeadm/main.go
@@ -77,7 +77,7 @@ var (
 	leaderElectionRenewDeadline time.Duration
 	leaderElectionRetryPeriod   time.Duration
 	watchFilterValue            string
-	watchNamespace              string
+	watchNamespacesList         []string
 	profilerAddress             string
 	enableContentionProfiling   bool
 	syncPeriod                  time.Duration
@@ -127,8 +127,8 @@ func InitFlags(fs *pflag.FlagSet) {
 	fs.DurationVar(&leaderElectionRetryPeriod, "leader-elect-retry-period", 5*time.Second,
 		"Duration the LeaderElector clients should wait between tries of actions (duration string)")
 
-	fs.StringVar(&watchNamespace, "namespace", "",
-		"Namespace that the controller watches to reconcile cluster-api objects. If unspecified, the controller watches for cluster-api objects across all namespaces.")
+	fs.StringSliceVar(&watchNamespacesList, "namespace", nil,
+		"Comma-separated list of namespaces that the controller watches to reconcile cluster-api objects. If unspecified, the controller watches for cluster-api objects across all namespaces.")
 
 	fs.StringVar(&watchFilterValue, "watch-filter", "",
 		fmt.Sprintf("Label value that the controller watches to reconcile cluster-api objects. Label key is always %s. If unspecified, the controller watches for all cluster-api objects.", clusterv1.WatchLabel))
@@ -235,9 +235,10 @@ func main() {
 	}
 
 	var watchNamespaces map[string]cache.Config
-	if watchNamespace != "" {
-		watchNamespaces = map[string]cache.Config{
-			watchNamespace: {},
+	if watchNamespacesList != nil {
+		watchNamespaces = map[string]cache.Config{}
+		for _, watchNamespace := range watchNamespacesList {
+			watchNamespaces[watchNamespace] = cache.Config{}
 		}
 	}
 
diff --git a/main.go b/main.go
index 919e0313f64f..ebc31657cf9d 100644
--- a/main.go
+++ b/main.go
@@ -98,7 +98,7 @@ var (
 	leaderElectionRenewDeadline time.Duration
 	leaderElectionRetryPeriod   time.Duration
 	watchFilterValue            string
-	watchNamespace              string
+	watchNamespacesList         []string
 	profilerAddress             string
 	enableContentionProfiling   bool
 	syncPeriod                  time.Duration
@@ -171,8 +171,8 @@ func InitFlags(fs *pflag.FlagSet) {
 	fs.DurationVar(&leaderElectionRetryPeriod, "leader-elect-retry-period", 2*time.Second,
 		"Duration the LeaderElector clients should wait between tries of actions (duration string)")
 
-	fs.StringVar(&watchNamespace, "namespace", "",
-		"Namespace that the controller watches to reconcile cluster-api objects. If unspecified, the controller watches for cluster-api objects across all namespaces.")
+	fs.StringSliceVar(&watchNamespacesList, "namespace", nil,
+		"Comma-separated list of namespaces that the controller watches to reconcile cluster-api objects. If unspecified, the controller watches for cluster-api objects across all namespaces.")
 
 	fs.StringVar(&watchFilterValue, "watch-filter", "",
 		fmt.Sprintf("Label value that the controller watches to reconcile cluster-api objects. Label key is always %s. If unspecified, the controller watches for all cluster-api objects.", clusterv1.WatchLabel))
@@ -321,9 +321,10 @@ func main() {
 	}
 
 	var watchNamespaces map[string]cache.Config
-	if watchNamespace != "" {
-		watchNamespaces = map[string]cache.Config{
-			watchNamespace: {},
+	if watchNamespacesList != nil {
+		watchNamespaces = map[string]cache.Config{}
+		for _, watchNamespace := range watchNamespacesList {
+			watchNamespaces[watchNamespace] = cache.Config{}
 		}
 	}
 
diff --git a/test/infrastructure/docker/main.go b/test/infrastructure/docker/main.go
index 425425c396a5..9720de0c01e8 100644
--- a/test/infrastructure/docker/main.go
+++ b/test/infrastructure/docker/main.go
@@ -77,7 +77,7 @@ var (
 	leaderElectionRenewDeadline time.Duration
 	leaderElectionRetryPeriod   time.Duration
 	watchFilterValue            string
-	watchNamespace              string
+	watchNamespacesList         []string
 	profilerAddress             string
 	enableContentionProfiling   bool
 	syncPeriod                  time.Duration
@@ -125,8 +125,8 @@ func InitFlags(fs *pflag.FlagSet) {
 	fs.DurationVar(&leaderElectionRetryPeriod, "leader-elect-retry-period", 2*time.Second,
 		"Duration the LeaderElector clients should wait between tries of actions (duration string)")
 
-	fs.StringVar(&watchNamespace, "namespace", "",
-		"Namespace that the controller watches to reconcile cluster-api objects. If unspecified, the controller watches for cluster-api objects across all namespaces.")
+	fs.StringSliceVar(&watchNamespacesList, "namespace", nil,
+		"Comma-separated list of namespaces that the controller watches to reconcile cluster-api objects. If unspecified, the controller watches for cluster-api objects across all namespaces.")
 
 	fs.StringVar(&watchFilterValue, "watch-filter", "",
 		fmt.Sprintf("Label value that the controller watches to reconcile cluster-api objects. Label key is always %s. If unspecified, the controller watches for all cluster-api objects.", clusterv1.WatchLabel))
@@ -218,9 +218,10 @@ func main() {
 	}
 
 	var watchNamespaces map[string]cache.Config
-	if watchNamespace != "" {
-		watchNamespaces = map[string]cache.Config{
-			watchNamespace: {},
+	if watchNamespacesList != nil {
+		watchNamespaces = map[string]cache.Config{}
+		for _, watchNamespace := range watchNamespacesList {
+			watchNamespaces[watchNamespace] = cache.Config{}
 		}
 	}