diff --git a/backend/pkg/kubeconfig/kubeconfig.go b/backend/pkg/kubeconfig/kubeconfig.go
index d652c3abedc..a080d7459a3 100644
--- a/backend/pkg/kubeconfig/kubeconfig.go
+++ b/backend/pkg/kubeconfig/kubeconfig.go
@@ -4,6 +4,7 @@ import (
 	"encoding/base64"
 	"errors"
 	"fmt"
+	"io/fs"
 	"net/http"
 	"net/http/httputil"
 	"net/url"
@@ -460,9 +461,23 @@ type ContextLoadError struct {
 // It returns an error if the file cannot be read.
 // It will return valid (contexts, ContextLoadErrors,nil) and errors if there are any errors in the file.
 func LoadContextsFromFile(kubeConfigPath string, source int) ([]Context, []ContextLoadError, error) {
+	// An empty path or a path that does not exist on disk is not an error
+	// condition for this loader: there is simply nothing to read. The
+	// in-cluster mode leaves KubeConfigPath empty, and the dynamic-cluster
+	// persistence file is absent on a fresh deployment until the user adds
+	// the first dynamic cluster. Treating both as ERRORs produced log
+	// spam reported in issues #4724 and #4401.
+	if kubeConfigPath == "" {
+		return nil, nil, nil
+	}
+
 	data, err := os.ReadFile(kubeConfigPath) //nolint:gosec
 	if err != nil {
-		return nil, nil, fmt.Errorf("error reading kubeconfig file: %v", err)
+		if errors.Is(err, fs.ErrNotExist) {
+			return nil, nil, nil
+		}
+
+		return nil, nil, fmt.Errorf("error reading kubeconfig file: %w", err)
 	}
 
 	skipProxySetup := source != KubeConfig
diff --git a/backend/pkg/kubeconfig/kubeconfig_test.go b/backend/pkg/kubeconfig/kubeconfig_test.go
index f54cc4b03ab..56619b63609 100644
--- a/backend/pkg/kubeconfig/kubeconfig_test.go
+++ b/backend/pkg/kubeconfig/kubeconfig_test.go
@@ -77,11 +77,28 @@ func TestLoadAndStoreKubeConfigs(t *testing.T) {
 		require.Equal(t, "minikube", ctx.Name)
 	})
 
-	t.Run("invalid_file", func(t *testing.T) {
-		kubeConfigFile := "invalid_kubeconfig"
+	t.Run("missing_file", func(t *testing.T) {
+		// Regression for issues #4724 and #4401: a kubeconfig path that does
+		// not exist on disk (in-cluster dynamic-cluster persistence file,
+		// fresh deployments) used to surface as an ERROR. It should now be
+		// treated as "no contexts to load".
+		err := kubeconfig.LoadAndStoreKubeConfigs(
+			contextStore, "missing_kubeconfig", kubeconfig.KubeConfig, nil,
+		)
+		require.NoError(t, err)
+	})
 
-		err := kubeconfig.LoadAndStoreKubeConfigs(contextStore, kubeConfigFile, kubeconfig.KubeConfig, nil)
-		require.Error(t, err)
+	t.Run("empty_path", func(t *testing.T) {
+		// Regression for issues #4724 and #4401: in-cluster mode leaves
+		// KubeConfigPath empty; passing "" should not error.
+		store := kubeconfig.NewContextStore()
+
+		err := kubeconfig.LoadAndStoreKubeConfigs(store, "", kubeconfig.KubeConfig, nil)
+		require.NoError(t, err)
+
+		contexts, err := store.GetContexts()
+		require.NoError(t, err)
+		require.Empty(t, contexts)
 	})
 }
 
@@ -95,13 +112,22 @@ func TestLoadContextsFromKubeConfigFile(t *testing.T) {
 		require.Equal(t, 2, len(contexts), "Expected 2 contexts from valid file")
 	})
 
-	t.Run("invalid_file", func(t *testing.T) {
-		kubeConfigFile := "invalid_kubeconfig"
+	t.Run("missing_file", func(t *testing.T) {
+		// Regression for issues #4724 and #4401. See TestLoadAndStoreKubeConfigs.
+		contexts, contextErrors, err := kubeconfig.LoadContextsFromFile(
+			"missing_kubeconfig", kubeconfig.KubeConfig,
+		)
+		require.NoError(t, err, "missing file is not an error condition")
+		require.Empty(t, contextErrors)
+		require.Empty(t, contexts)
+	})
 
-		contexts, contextErrors, err := kubeconfig.LoadContextsFromFile(kubeConfigFile, kubeconfig.KubeConfig)
-		require.Error(t, err, "Expected error for invalid file")
-		require.Empty(t, contextErrors, "Expected no context errors for invalid file")
-		require.Empty(t, contexts, "Expected no contexts from invalid file")
+	t.Run("empty_path", func(t *testing.T) {
+		// Regression for issues #4724 and #4401: in-cluster mode passes "".
+		contexts, contextErrors, err := kubeconfig.LoadContextsFromFile("", kubeconfig.KubeConfig)
+		require.NoError(t, err)
+		require.Empty(t, contextErrors)
+		require.Empty(t, contexts)
 	})
 
 	t.Run("autherror", func(t *testing.T) {