diff --git a/changelog/861.feature.rst b/changelog/861.feature.rst
new file mode 100644
index 00000000..b04d252e
--- /dev/null
+++ b/changelog/861.feature.rst
@@ -0,0 +1 @@
+Show more helpful error message for invalid metadata.
diff --git a/tests/test_package.py b/tests/test_package.py
index 62108b5d..3d2e2799 100644
--- a/tests/test_package.py
+++ b/tests/test_package.py
@@ -337,23 +337,46 @@ def test_fips_metadata_excludes_md5_and_blake2(monkeypatch):
     assert "blake2_256_digest" not in mddict
 
 
-def test_pkginfo_returns_no_metadata(monkeypatch):
+@pytest.mark.parametrize(
+    "read_data, missing_fields",
+    [
+        pytest.param(
+            b"Metadata-Version: 2.3\nName: test-package\nVersion: 1.0.0\n",
+            "Name, Version",
+            id="unsupported Metadata-Version",
+        ),
+        pytest.param(
+            b"Metadata-Version: 2.2\nName: UNKNOWN\nVersion: UNKNOWN\n",
+            "Name, Version",
+            id="missing Name and Version",
+        ),
+        pytest.param(
+            b"Metadata-Version: 2.2\nName: UNKNOWN\nVersion: 1.0.0\n",
+            "Name",
+            id="missing Name",
+        ),
+        pytest.param(
+            b"Metadata-Version: 2.2\nName: test-package\nVersion: UNKNOWN\n",
+            "Version",
+            id="missing Version",
+        ),
+    ],
+)
+def test_pkginfo_returns_no_metadata(read_data, missing_fields, monkeypatch):
     """Raise an exception when pkginfo can't interpret the metadata.
 
     This could be caused by a version number or format it doesn't support yet.
     """
-
-    def EmptyDist(filename):
-        return pretend.stub(name=None, version=None)
-
-    monkeypatch.setattr(package_file, "DIST_TYPES", {"bdist_wheel": EmptyDist})
+    monkeypatch.setattr(package_file.wheel.Wheel, "read", lambda _: read_data)
     filename = "tests/fixtures/twine-1.5.0-py2.py3-none-any.whl"
 
     with pytest.raises(exceptions.InvalidDistribution) as err:
         package_file.PackageFile.from_filename(filename, comment=None)
 
-    assert "Invalid distribution metadata" in err.value.args[0]
-    assert "1.0, 1.1, 1.2, 2.0, 2.1, and 2.2" in err.value.args[0]
+    assert (
+        f"Metadata is missing required fields: {missing_fields}." in err.value.args[0]
+    )
+    assert "1.0, 1.1, 1.2, 2.0, 2.1, 2.2" in err.value.args[0]
 
 
 def test_malformed_from_file(monkeypatch):
diff --git a/twine/package.py b/twine/package.py
index da468a89..0619ba6e 100644
--- a/twine/package.py
+++ b/twine/package.py
@@ -101,15 +101,21 @@ def from_filename(cls, filename: str, comment: Optional[str]) -> "PackageFile":
                 "Unknown distribution format: '%s'" % os.path.basename(filename)
             )
 
-        # If pkginfo encounters a metadata version it doesn't support, it may
-        # give us back empty metadata. At the very least, we should have a name
-        # and version
-        if not (meta.name and meta.version):
+        # If pkginfo encounters a metadata version it doesn't support, it may give us
+        # back empty metadata. At the very least, we should have a name and version,
+        # which could also be empty if, for example, a MANIFEST.in doesn't include
+        # setup.cfg.
+        missing_fields = [
+            f.capitalize() for f in ["name", "version"] if not getattr(meta, f)
+        ]
+        if missing_fields:
             supported_metadata = list(pkginfo.distribution.HEADER_ATTRS)
             raise exceptions.InvalidDistribution(
-                "Invalid distribution metadata. "
-                "This version of twine supports Metadata-Version "
-                f"{', '.join(supported_metadata[:-1])}, and {supported_metadata[-1]}"
+                "Metadata is missing required fields: "
+                f"{', '.join(missing_fields)}.\n"
+                "Make sure the distribution includes the files where those fields "
+                "are specified, and is using a supported Metadata-Version: "
+                f"{', '.join(supported_metadata)}."
             )
 
         py_version: Optional[str]