diff --git a/pulp_container/app/serializers.py b/pulp_container/app/serializers.py
index 6a767d857..4b8e46ce6 100644
--- a/pulp_container/app/serializers.py
+++ b/pulp_container/app/serializers.py
@@ -798,9 +798,12 @@ def validate(self, data):
         """Validates that all the fields make sense."""
         data = super().validate(data)
 
-        if bool(data.get("containerfile", None)) == bool(data.get("containerfile_name", None)):
+        # only one of containerfile or containerfile_name should be provided, none of them is ok
+        # in case we have a build_context because Pulp will try to find a file called Containerfile
+        # in the build_context provided
+        if data.get("containerfile", None) and data.get("containerfile_name", None):
             raise serializers.ValidationError(
-                _("Exactly one of 'containerfile' or 'containerfile_name' must be specified.")
+                _("Only one of 'containerfile' or 'containerfile_name' must be specified.")
             )
 
         if "containerfile_name" in data and "build_context" not in data:
@@ -808,6 +811,20 @@ def validate(self, data):
                 _("A 'build_context' must be specified when 'containerfile_name' is present.")
             )
 
+        # with none of build_context nor containerfile_name nor containerfile
+        # there is not enough information to build
+        if not (
+            data.get("containerfile", None)
+            or data.get("containerfile_name", None)
+            or data.get("build_context", None)
+        ):
+            raise serializers.ValidationError(
+                _(
+                    "At least one of 'build_context' or 'containerfile' or 'containerfile_name' "
+                    "must be provided"
+                )
+            )
+
         # TODO: this can be removed after https://github.com/pulp/pulpcore/issues/5786
         if data.get("build_context", None):
             data["repository_version"] = data["build_context"]
@@ -821,6 +838,12 @@ def deferred_files_validation(self, data):
         """
         if build_context := data.get("build_context", None):
 
+            data["build_context_pk"] = build_context.repository.pk
+
+            # if a containerfile was passed with the build_context we can skip the following checks
+            if data.get("containerfile", None):
+                return data
+
             # check if the on_demand_artifacts exist
             for on_demand_artifact in build_context.on_demand_artifacts.iterator():
                 if not on_demand_artifact.content_artifact.artifact:
@@ -831,7 +854,7 @@ def deferred_files_validation(self, data):
                         )
                     )
 
-            # check if the containerfile_name exists in the build_context (File Repository)
+            # check if the provided containerfile_name exists in the build_context (File Repository)
             if (
                 data.get("containerfile_name", None)
                 and not FileContent.objects.filter(
@@ -847,7 +870,21 @@ def deferred_files_validation(self, data):
                     )
                 )
 
-            data["build_context_pk"] = build_context.repository.pk
+            # check if a Containerfile exists in the build_context when
+            # no containerfile_name is provided
+            if (
+                not data.get("containerfile_name", None)
+                and not FileContent.objects.filter(
+                    repositories__in=[build_context.repository.pk],
+                    relative_path="Containerfile",
+                ).exists()
+            ):
+                raise serializers.ValidationError(
+                    _("Could not find the Containerfile in the build_context provided")
+                )
+
+            if not data.get("containerfile_name", None):
+                data["containerfile_name"] = "Containerfile"
 
         return data
 
diff --git a/pulp_container/tests/functional/api/test_build_images.py b/pulp_container/tests/functional/api/test_build_images.py
index 3980246b0..7eb350cae 100644
--- a/pulp_container/tests/functional/api/test_build_images.py
+++ b/pulp_container/tests/functional/api/test_build_images.py
@@ -140,15 +140,31 @@ def test_build_image_from_repo_version_with_creator_user(
 
 def test_build_image_without_containerfile(
     build_image,
+    check_manifest_fields,
+    container_distribution_api,
     container_repo,
+    delete_orphans_pre,
+    gen_object_with_cleanup,
+    local_registry,
     populated_file_repo,
 ):
-    """Test build an OCI image without a containerfile"""
-    with pytest.raises(ApiException):
-        build_image(
-            repository=container_repo.pulp_href,
-            build_context=f"{populated_file_repo.pulp_href}versions/2/",
-        )
+    """Test build an OCI image without explicitly passing a Containerfile"""
+    build_image(
+        repository=container_repo.pulp_href,
+        build_context=f"{populated_file_repo.pulp_href}versions/2/",
+    )
+
+    distribution = gen_object_with_cleanup(
+        container_distribution_api,
+        ContainerContainerDistribution(**gen_distribution(repository=container_repo.pulp_href)),
+    )
+
+    local_registry.pull(distribution.base_path)
+    image = local_registry.inspect(distribution.base_path)
+    assert image[0]["Config"]["Cmd"] == ["cat", "/tmp/inside-image.txt"]
+    assert check_manifest_fields(
+        manifest_filters={"digest": image[0]["Digest"]}, fields={"type": MANIFEST_TYPE.IMAGE}
+    )
 
 
 def test_build_image_without_expected_files(
@@ -237,3 +253,22 @@ def containerfile_without_context_files():
     local_registry.pull(distribution.base_path)
     image = local_registry.inspect(distribution.base_path)
     assert image[0]["Config"]["Cmd"] == ["ls", "/"]
+
+
+def test_with_containerfilename_and_containerfile(
+    build_image,
+    containerfile_name,
+    container_repo,
+    delete_orphans_pre,
+    populated_file_repo,
+):
+    """Test build an OCI image with a containerfile and containerfile_name"""
+    with pytest.raises(ApiException) as e:
+        build_image(
+            repository=container_repo.pulp_href,
+            containerfile_name="Non_existing_file",
+            containerfile=containerfile_name,
+            build_context=f"{populated_file_repo.pulp_href}versions/2/",
+        )
+    assert e.value.status == 400
+    assert "Only one of 'containerfile' or 'containerfile_name' must be specified." in e.value.body