diff --git a/RELEASE_NOTES.md b/RELEASE_NOTES.md
index 20b3ff64..437a6538 100644
--- a/RELEASE_NOTES.md
+++ b/RELEASE_NOTES.md
@@ -22,6 +22,7 @@
 * [#374](https://github.com/suse-edge/edge-image-builder/issues/374) - Enable SELinux support for Kubernetes agents if servers enforce it
 * [#381](https://github.com/suse-edge/edge-image-builder/issues/381) - Empty gpg-keys directory passes GPG enablement only to fail during the dependency resolution
 * [#383](https://github.com/suse-edge/edge-image-builder/issues/383) - Criteria for validating the OS definition does not include RPM
+* [#372](https://github.com/suse-edge/edge-image-builder/issues/372) -  Empty certificates directory does not raise a build error but fails to boot the node
 
 ---
 
diff --git a/pkg/combustion/certificates.go b/pkg/combustion/certificates.go
index 4049d042..2b49d814 100644
--- a/pkg/combustion/certificates.go
+++ b/pkg/combustion/certificates.go
@@ -47,6 +47,15 @@ func copyCertificates(ctx *image.Context) error {
 	srcDir := filepath.Join(ctx.ImageConfigDir, certsConfigDir)
 	destDir := filepath.Join(ctx.CombustionDir, certsConfigDir)
 
+	dirEntries, err := os.ReadDir(srcDir)
+	if err != nil {
+		return fmt.Errorf("reading the certificates directory at %s: %w", srcDir, err)
+	}
+
+	if len(dirEntries) == 0 {
+		return fmt.Errorf("no certificates found in directory %s", srcDir)
+	}
+
 	if err := os.MkdirAll(destDir, os.ModePerm); err != nil {
 		return fmt.Errorf("creating certificates directory '%s': %w", destDir, err)
 	}
diff --git a/pkg/combustion/certificates_test.go b/pkg/combustion/certificates_test.go
index f63b5c22..1f2305fa 100644
--- a/pkg/combustion/certificates_test.go
+++ b/pkg/combustion/certificates_test.go
@@ -28,6 +28,23 @@ func setupCertificatesConfigDir(t *testing.T) (ctx *image.Context, teardown func
 	return
 }
 
+func TestCopyCertificatesEmptyDirectory(t *testing.T) {
+	// Setup
+	ctx, teardown := setupContext(t)
+	defer teardown()
+
+	testCertsDir := filepath.Join(ctx.ImageConfigDir, certsConfigDir)
+	err := os.Mkdir(testCertsDir, 0o755)
+	require.NoError(t, err)
+	defer os.RemoveAll(testCertsDir)
+
+	// Test
+	err = copyCertificates(ctx)
+
+	// Verify
+	require.Error(t, err)
+}
+
 func TestCopyCertificates(t *testing.T) {
 	// Setup
 	ctx, teardown := setupCertificatesConfigDir(t)