diff --git a/src/bentoml/_internal/container/generate.py b/src/bentoml/_internal/container/generate.py
index 0b0e8b26934..feb645b8838 100644
--- a/src/bentoml/_internal/container/generate.py
+++ b/src/bentoml/_internal/container/generate.py
@@ -181,7 +181,9 @@ def generate_containerfile(
 
     user_templates = docker.dockerfile_template
     if user_templates is not None:
-        dir_path = os.path.dirname(resolve_user_filepath(user_templates, build_ctx))
+        dir_path = os.path.dirname(
+            resolve_user_filepath(user_templates, build_ctx, secure=False)
+        )
         user_templates = os.path.basename(user_templates)
         TEMPLATES_PATH.append(dir_path)
         environment = ENVIRONMENT.overlay(
diff --git a/tests/unit/_internal/container/test_generate.py b/tests/unit/_internal/container/test_generate.py
index e39364671e3..427fb17d40a 100644
--- a/tests/unit/_internal/container/test_generate.py
+++ b/tests/unit/_internal/container/test_generate.py
@@ -5,6 +5,30 @@
 from bentoml._internal.container.generate import generate_containerfile
 
 
+def test_generate_containerfile_dockerfile_template_outside_cwd(tmp_path) -> None:
+    # Regression test for https://github.com/bentoml/BentoML/issues/5566.
+    # During `bentoml containerize` the build context is a BentoML-managed temp
+    # directory (not under os.getcwd()), so resolve_user_filepath must be called
+    # with secure=False — otherwise it raises ValueError for any /tmp path.
+    template_dir = tmp_path / "env" / "docker"
+    template_dir.mkdir(parents=True)
+    (template_dir / "Dockerfile.template").write_text(
+        "{% extends bento_base_template %}\n"
+    )
+
+    # Must not raise ValueError even though tmp_path is outside os.getcwd()
+    generate_containerfile(
+        DockerOptions(
+            distro="debian",
+            python_version="3.11",
+            dockerfile_template="env/docker/Dockerfile.template",
+        ),
+        str(tmp_path),
+        conda=CondaOptions(),
+        bento_fs=tmp_path,
+    )
+
+
 def test_generate_containerfile_quotes_system_packages(tmp_path) -> None:
     dockerfile = generate_containerfile(
         DockerOptions(