diff --git a/tests/test_metadata_serialization.py b/tests/test_metadata_serialization.py
index 3714eec00c..f116d33326 100644
--- a/tests/test_metadata_serialization.py
+++ b/tests/test_metadata_serialization.py
@@ -44,8 +44,8 @@ class TestSerialization(unittest.TestCase):
         "_type wrong type": '{"_type": "foo", "spec_version": "1.0.0", "version": 1, "expires": "2030-01-01T00:00:00Z", "meta": {}}',
         "version wrong type": '{"_type": "signed", "spec_version": "1.0.0", "version": "a", "expires": "2030-01-01T00:00:00Z", "meta": {}}',
         "invalid spec_version str": '{"_type": "signed", "spec_version": "abc", "version": 1, "expires": "2030-01-01T00:00:00Z", "meta": {}}',
-        "two digit spec_version": '{"_type": "signed", "spec_version": "1.2.a", "version": 1, "expires": "2030-01-01T00:00:00Z", "meta": {}}',
-        "no digit spec_version": '{"_type": "signed", "spec_version": "a.b.c", "version": 1, "expires": "2030-01-01T00:00:00Z", "meta": {}}',
+        "non-number spec_version": '{"_type": "signed", "spec_version": "1.2.a", "version": 1, "expires": "2030-01-01T00:00:00Z", "meta": {}}',
+        "one part spec_version": '{"_type": "signed", "spec_version": "1", "version": 1, "expires": "2030-01-01T00:00:00Z", "meta": {}}',
         "different major spec_version": '{"_type": "signed", "spec_version": "0.0.0", "version": 1, "expires": "2030-01-01T00:00:00Z", "meta": {}}',
         "version 0": '{"_type": "signed", "spec_version": "1.0.0", "version": 0, "expires": "2030-01-01T00:00:00Z", "meta": {}}',
         "version below 0": '{"_type": "signed", "spec_version": "1.0.0", "version": -1, "expires": "2030-01-01T00:00:00Z", "meta": {}}',
@@ -254,6 +254,8 @@ def test_invalid_timestamp_serialization(self, test_case_data: str) -> None:
     valid_timestamps: utils.DataSet = {
         "all": '{ "_type": "timestamp", "spec_version": "1.0.0", "version": 1, "expires": "2030-01-01T00:00:00Z", \
             "meta": {"snapshot.json": {"hashes": {"sha256" : "abc"}, "version": 1}}}',
+        "two part spec_version": '{ "_type": "timestamp", "spec_version": "1.9000", "version": 1, "expires": "2030-01-01T00:00:00Z", \
+            "meta": {"snapshot.json": {"hashes": {"sha256" : "abc"}, "version": 1}}}',
         "unrecognized field": '{ "_type": "timestamp", "spec_version": "1.0.0", "version": 1, "expires": "2030-01-01T00:00:00Z", \
             "meta": {"snapshot.json": {"hashes": {"sha256" : "abc"}, "version": 1}}, "foo": "bar"}',
     }
diff --git a/tuf/api/metadata.py b/tuf/api/metadata.py
index cd73985e8c..ce552fad83 100644
--- a/tuf/api/metadata.py
+++ b/tuf/api/metadata.py
@@ -431,16 +431,18 @@ def __init__(
         expires: datetime,
         unrecognized_fields: Optional[Mapping[str, Any]] = None,
     ):
+        # Accept semver (X.Y.Z) but also X.Y for legacy compatibility
         spec_list = spec_version.split(".")
         if (
-            len(spec_list) != 3
+            len(spec_list) not in [2, 3]
             or not all(el.isdigit() for el in spec_list)
-            or spec_list[0] != SPECIFICATION_VERSION[0]
         ):
-            raise ValueError(
-                f"Unsupported spec_version, got {spec_list}, "
-                f"supported {'.'.join(SPECIFICATION_VERSION)}"
-            )
+            raise ValueError(f"Failed to parse spec_version {spec_version}")
+
+        # major version must match
+        if spec_list[0] != SPECIFICATION_VERSION[0]:
+            raise ValueError(f"Unsupported spec_version {spec_version}")
+
         self.spec_version = spec_version
         self.expires = expires