diff --git a/tmt/cli.py b/tmt/cli.py
index 98fbfd798e..d31781964b 100644
--- a/tmt/cli.py
+++ b/tmt/cli.py
@@ -773,7 +773,7 @@ def tests_import(
 # TODO: move to `template` export plugin options
 @option(
     '--template', metavar='PATH',
-    help="Path to a template to use for rendering the export. Used with '--how=template' only."
+    help="Path to a template to use for rendering the export. Used with '--how=rst|template' only."
     )
 def tests_export(
         context: Context,
@@ -1004,7 +1004,7 @@ def plans_create(
 # TODO: move to `template` export plugin options
 @option(
     '--template', metavar='PATH',
-    help="Path to a template to use for rendering the export. Used with '--how=template' only."
+    help="Path to a template to use for rendering the export. Used with '--how=rst|template' only."
     )
 def plans_export(
         context: Context,
@@ -1260,7 +1260,7 @@ def headfoot(text: str) -> None:
 # TODO: move to `template` export plugin options
 @option(
     '--template', metavar='PATH',
-    help="Path to a template to use for rendering the export. Used with '--how=template' only."
+    help="Path to a template to use for rendering the export. Used with '--how=rst|template' only."
     )
 def stories_export(
         context: Context,
diff --git a/tmt/export/rst.py b/tmt/export/rst.py
index 90d19337ba..80dd85689c 100644
--- a/tmt/export/rst.py
+++ b/tmt/export/rst.py
@@ -4,6 +4,7 @@
 import tmt.export
 import tmt.export.template
 import tmt.utils
+from tmt.utils import Path
 
 
 @tmt.base.Story.provides_export('rst')
@@ -12,8 +13,10 @@ class RestructuredExporter(tmt.export.ExportPlugin):
     def export_story(cls,
                      story: tmt.base.Story,
                      keys: Optional[List[str]] = None,
+                     template: Optional[Path] = None,
                      include_title: bool = True) -> str:
         return tmt.export.template.TemplateExporter.render_template(
+            template_filepath=template,
             default_template_filename='default-story.rst.j2',
             keys=keys,
             STORY=story,
@@ -23,7 +26,9 @@ def export_story(cls,
     def export_story_collection(cls,
                                 stories: List[tmt.base.Story],
                                 keys: Optional[List[str]] = None,
+                                template: Optional[Path] = None,
                                 include_title: bool = True,
                                 **kwargs: Any) -> str:
-        return '\n\n'.join([cls.export_story(story, keys=keys, include_title=include_title)
-                           for story in stories])
+        return '\n\n'.join([
+            cls.export_story(story, keys=keys, template=template, include_title=include_title)
+            for story in stories])
diff --git a/tmt/utils.py b/tmt/utils.py
index 4e274aafe3..951e8ce53f 100644
--- a/tmt/utils.py
+++ b/tmt/utils.py
@@ -5142,6 +5142,10 @@ def render_template_file(
 
         return template.render(**variables).strip()
 
+    except FileNotFoundError as exc:
+        raise GeneralError(
+            f"Could not open template '{template_filepath}'.") from exc
+
     except jinja2.exceptions.TemplateSyntaxError as exc:
         raise GeneralError(
             f"Could not parse template '{template_filepath}' at line {exc.lineno}.") from exc