diff --git a/docs/configuration.rst b/docs/configuration.rst
index e7c8a99d..0a350691 100644
--- a/docs/configuration.rst
+++ b/docs/configuration.rst
@@ -80,6 +80,8 @@ Top level keys
 
     ``""`` by default.
 
+    Formatted titles are appended a line of ``=`` on the following line (reStructuredText title format) unless the template has an ``.md`` suffix, in which case the title will instead be prefixed with ``#`` (markdown title format).
+
 ``issue_format``
     A format string for rendering the issue/ticket number in newsfiles.
 
diff --git a/src/towncrier/build.py b/src/towncrier/build.py
index b28606c9..e0add371 100644
--- a/src/towncrier/build.py
+++ b/src/towncrier/build.py
@@ -170,8 +170,11 @@ def __main(
             .joinpath(config.template[1])
             .read_text(encoding="utf-8")
         )
+        template_extension = os.path.splitext(config.template[1])[1]
     else:
         template = Path(config.template).read_text(encoding="utf-8")
+        template_extension = os.path.splitext(config.template)[1]
+    is_markdown = template_extension.lower() == ".md"
 
     click.echo("Finding news fragments...", err=to_err)
 
@@ -215,22 +218,10 @@ def __main(
     if project_date is None:
         project_date = _get_date().strip()
 
-    if config.title_format:
-        top_line = config.title_format.format(
-            name=project_name, version=project_version, project_date=project_date
-        )
-        render_title_with_fragments = False
-        render_title_separately = True
-    elif config.title_format is False:
-        # This is an odd check but since we support both "" and False with
-        # different effects we have to do something a bit abnormal here.
-        top_line = ""
-        render_title_separately = False
-        render_title_with_fragments = False
-    else:
-        top_line = ""
-        render_title_separately = False
-        render_title_with_fragments = True
+    # Render the title in the template if the title format is set to "". It can
+    # alternatively be set to False or a string, in either case it shouldn't be rendered
+    # in the template.
+    render_title = config.title_format == ""
 
     rendered = render_fragments(
         # The 0th underline is used for the top line
@@ -243,18 +234,21 @@ def __main(
         {"name": project_name, "version": project_version, "date": project_date},
         top_underline=config.underlines[0],
         all_bullets=config.all_bullets,
-        render_title=render_title_with_fragments,
+        render_title=render_title,
     )
 
-    if render_title_separately:
-        content = "\n".join(
-            [
-                top_line,
-                config.underlines[0] * len(top_line),
-                rendered,
-            ]
+    if config.title_format:
+        top_line = config.title_format.format(
+            name=project_name, version=project_version, project_date=project_date
         )
+        if is_markdown:
+            parts = [f"# {top_line}"]
+        else:
+            parts = [top_line, config.underlines[0] * len(top_line)]
+        parts.append(rendered)
+        content = "\n".join(parts)
     else:
+        top_line = ""
         content = rendered
 
     if draft:
diff --git a/src/towncrier/newsfragments/610.feature.rst b/src/towncrier/newsfragments/610.feature.rst
new file mode 100644
index 00000000..5b76ab2c
--- /dev/null
+++ b/src/towncrier/newsfragments/610.feature.rst
@@ -0,0 +1 @@
+The ``title_format`` configuration option now uses a markdown format for markdown templates.
diff --git a/src/towncrier/test/test_build.py b/src/towncrier/test/test_build.py
index 17ffad49..23cfb860 100644
--- a/src/towncrier/test/test_build.py
+++ b/src/towncrier/test/test_build.py
@@ -1032,6 +1032,56 @@ def test_title_format_custom(self, runner):
 
 
 
+        """
+        )
+
+        self.assertEqual(0, result.exit_code)
+        self.assertEqual(expected_output, result.output)
+
+    @with_project(
+        config="""
+        [tool.towncrier]
+        package = "foo"
+        filename = "NEWS.md"
+        title_format = "[{project_date}] CUSTOM RELEASE for {name} version {version}"
+        """
+    )
+    def test_title_format_custom_markdown(self, runner):
+        """
+        A non-empty title format adds the specified title, and if the target filename is
+        markdown then the title is added as a markdown header.
+        """
+        with open("foo/newsfragments/123.feature", "w") as f:
+            f.write("Adds levitation")
+        result = runner.invoke(
+            _main,
+            [
+                "--name",
+                "FooBarBaz",
+                "--version",
+                "7.8.9",
+                "--date",
+                "20-01-2001",
+                "--draft",
+            ],
+        )
+
+        expected_output = dedent(
+            """\
+            Loading template...
+            Finding news fragments...
+            Rendering news fragments...
+            Draft only -- nothing has been written.
+            What is seen below is what would be written.
+
+            # [20-01-2001] CUSTOM RELEASE for FooBarBaz version 7.8.9
+
+            ### Features
+
+            - Adds levitation (#123)
+
+
+
         """
         )