diff --git a/pkg/restapi/cluster.go b/pkg/restapi/cluster.go
index cd1cd7ae38..3be459e127 100644
--- a/pkg/restapi/cluster.go
+++ b/pkg/restapi/cluster.go
@@ -149,6 +149,9 @@ func (h clusterHandler) updateCluster(w http.ResponseWriter, r *http.Request) {
 		return
 	}
 	newCluster.ID = c.ID
+	// Cluster.KnownHosts are not part of REST API definitions,
+	// so we need to fill them based on current cluster state.
+	newCluster.KnownHosts = c.KnownHosts
 
 	if err := h.svc.PutCluster(r.Context(), newCluster); err != nil {
 		respondError(w, r, errors.Wrapf(err, "update cluster %q", c.ID))
diff --git a/pkg/service/cluster/service.go b/pkg/service/cluster/service.go
index 60a929bbae..e2167b0b44 100644
--- a/pkg/service/cluster/service.go
+++ b/pkg/service/cluster/service.go
@@ -442,6 +442,17 @@ func (s *Service) PutCluster(ctx context.Context, c *Cluster) (err error) {
 		s.logger.Info(ctx, "Adding new cluster", "cluster_id", c.ID)
 	} else {
 		s.logger.Info(ctx, "Updating cluster", "cluster_id", c.ID)
+		// Putting cluster should theoretically just set cluster state to the provided one.
+		// The problem is that Cluster.KnownHosts are not part of REST API definitions,
+		// so it's possible that cluster passed to PutCluster doesn't have it set by accident.
+		// This shouldn't be the case, but since it never makes sense for Cluster.KnownHosts
+		// to be empty (they should at least contain resolved Cluster.Host), we can add additional
+		// safety net here and load them if they are missing.
+		if len(c.KnownHosts) == 0 {
+			if err := s.loadKnownHosts(c); err != nil && !errors.Is(err, gocql.ErrNotFound) {
+				return errors.Wrap(err, "load known hosts")
+			}
+		}
 	}
 
 	// Validate cluster model
diff --git a/pkg/service/cluster/service_integration_test.go b/pkg/service/cluster/service_integration_test.go
index 7a9264983a..571c4463e5 100644
--- a/pkg/service/cluster/service_integration_test.go
+++ b/pkg/service/cluster/service_integration_test.go
@@ -850,25 +850,45 @@ func TestServiceStorageIntegration(t *testing.T) {
 		if err = s.PutCluster(ctx, &initialCluster); err != nil {
 			t.Fatal(err)
 		}
+		Print("Known hosts are set after cluster creation")
+		getCluster, err := s.GetClusterByID(t.Context(), initialCluster.ID)
+		if err != nil {
+			t.Fatal(err)
+		}
+		if len(getCluster.KnownHosts) != len(hosts) {
+			t.Fatalf("Expected %d known hosts, got %d", len(hosts), len(getCluster.KnownHosts))
+		}
 
-		unavailableHost := hosts[1]
-		Print("Block connectivity to host: " + unavailableHost)
-		if err := RunIptablesCommand(t, unavailableHost, CmdBlockScyllaREST); err != nil {
+		Print("Block connectivity to host: " + clusterHost)
+		if err := RunIptablesCommand(t, clusterHost, CmdBlockScyllaREST); err != nil {
 			t.Fatal(err)
 		}
-		defer RunIptablesCommand(t, unavailableHost, CmdUnblockScyllaREST)
+		defer RunIptablesCommand(t, clusterHost, CmdUnblockScyllaREST)
 
 		Print("Expect connectivity failure when adding new cluster")
 		putCluster := *validCluster()
 		putCluster.Host = clusterHost
+		// Simulate missing known hosts and expect that
+		// they won't overwrite existing known hosts.
+		putCluster.KnownHosts = nil
 		if err := s.PutCluster(ctx, &putCluster); err == nil {
 			t.Fatal("Expected connectivity failure when adding new cluster, got nil")
 		}
 
-		newClusterHost := hosts[2]
+		Print("Known hosts are set after failed cluster update")
+		getCluster, err = s.GetClusterByID(t.Context(), initialCluster.ID)
+		if err != nil {
+			t.Fatal(err)
+		}
+		if len(getCluster.KnownHosts) != len(hosts) {
+			t.Fatalf("Expected %d known hosts, got %d", len(hosts), len(getCluster.KnownHosts))
+		}
+
+		newClusterHost := hosts[1]
 		Print("Expect connectivity failure when updating existing cluster host param: " + newClusterHost)
 		putCluster = initialCluster
 		putCluster.Host = newClusterHost
+		putCluster.KnownHosts = nil
 		if err := s.PutCluster(ctx, &putCluster); err == nil {
 			t.Fatal("Expected connectivity failure when updating existing cluster host param, got nil")
 		}
@@ -876,9 +896,19 @@ func TestServiceStorageIntegration(t *testing.T) {
 		Print("Expect success when updating existing cluster labels param")
 		putCluster = initialCluster
 		putCluster.Labels = map[string]string{"foo": "bar"}
+		putCluster.KnownHosts = nil
 		if err := s.PutCluster(ctx, &putCluster); err != nil {
 			t.Fatal(err)
 		}
+
+		Print("Known hosts are set after successful cluster update")
+		getCluster, err = s.GetClusterByID(t.Context(), initialCluster.ID)
+		if err != nil {
+			t.Fatal(err)
+		}
+		if len(getCluster.KnownHosts) != len(hosts) {
+			t.Fatalf("Expected %d known hosts, got %d", len(hosts), len(getCluster.KnownHosts))
+		}
 	})
 
 	t.Run("no --host in SM DB", func(t *testing.T) {