diff --git a/datasette/schema_watcher.py b/datasette/schema_watcher.py
index ea7be2ea..6fa5ed7f 100644
--- a/datasette/schema_watcher.py
+++ b/datasette/schema_watcher.py
@@ -71,6 +71,9 @@ SCAN_CONCURRENCY = 1
 # sweep with os.scandir() instead of probing -wal/-journal with stat()
 SCANDIR_THRESHOLD = 8
 PRAGMA_BUSY_TIMEOUT_MS = 200
+# Read the schema cookie from the file header instead of opening a
+# connection when no -wal/-journal has content
+USE_HEADER_CHECK = True
 
 
 class WatchState:
@@ -171,6 +174,35 @@ def is_racy(fp, t_ns):
     return newest_timestamp(fp) >= t_ns - RACY_WINDOW_NS
 
 
+SQLITE_HEADER = b"SQLite format 3\x00"
+
+
+def header_schema_version(path):
+    """The schema cookie (offset 40 of the database header) read straight
+    from the file - what PRAGMA schema_version returns - without opening a
+    SQLite connection or taking any lock.
+
+    Only meaningful when there is no non-empty -wal or -journal: then the
+    main file is the whole database. The caller must have taken the
+    fingerprint *before* calling this; a commit in flight at that moment has
+    already bumped the mtime it saw, so the fingerprint is racy and the next
+    sweep looks again.
+    """
+    try:
+        fd = os.open(path, os.O_RDONLY)
+    except OSError:
+        return None
+    try:
+        header = os.pread(fd, 100, 0)
+    except OSError:
+        return None
+    finally:
+        os.close(fd)
+    if len(header) < 100 or not header.startswith(SQLITE_HEADER):
+        return None
+    return int.from_bytes(header[40:44], "big")
+
+
 def _fp_to_json(fp, t_ns):
     return json.dumps({"fp": fp, "t": t_ns})
 
@@ -198,6 +230,7 @@ class SchemaWatcher:
             "sweep_seconds": 0.0,
             "stats": 0,
             "pragma_checks": 0,
+            "header_checks": 0,
             "scans": 0,
             "write_detections": 0,
             "replaced": 0,
@@ -476,8 +509,10 @@ class SchemaWatcher:
             elif kind == "busy":
                 self.counters["busy"] += 1
                 state.fp_racy = True  # check again next sweep
-            elif kind == "checked":
-                self.counters["pragma_checks"] += 1
+            elif kind in ("checked", "header"):
+                self.counters[
+                    "pragma_checks" if kind == "checked" else "header_checks"
+                ] += 1
                 state.stats["checks"] += 1
                 if version != state.catalog_version:
                     state.needs_scan = True
@@ -525,6 +560,14 @@ class SchemaWatcher:
                     # first sight: the schema_version alone cannot be trusted
                     out.append((state, "replaced", fp, t_ns, None))
                     continue
+                if USE_HEADER_CHECK and fp[1] is None and fp[2] is None:
+                    # No -wal/-journal content: read the cookie from the
+                    # header. No connection, no SHARED lock that could make
+                    # a concurrent writer back off.
+                    version = header_schema_version(os.fspath(state.db.path))
+                    if version is not None:
+                        out.append((state, "header", fp, t_ns, version))
+                        continue
                 out.append(self._pragma_check(state, fp, t_ns))
         return out
 
diff --git a/tests/test_schema_watcher.py b/tests/test_schema_watcher.py
index 2f26f79d..2b876809 100644
--- a/tests/test_schema_watcher.py
+++ b/tests/test_schema_watcher.py
@@ -229,7 +229,9 @@ async def test_external_data_only_insert_does_not_rescan(db_path):
 
 
 @pytest.mark.asyncio
-async def test_external_add_column(db_path):
+@pytest.mark.parametrize("use_header", (True, False))
+async def test_external_add_column(db_path, monkeypatch, use_header):
+    monkeypatch.setattr(schema_watcher_module, "USE_HEADER_CHECK", use_header)
     ds = await start_ds([db_path])
     run_external(db_path, "alter table t add column b text")
 
@@ -395,11 +397,41 @@ def _coarse_fingerprint(real):
     return fingerprint
 
 
+@pytest.mark.parametrize("journal_mode", ("delete", "wal", "truncate"))
+def test_header_schema_version_matches_pragma(tmp_path, journal_mode):
+    path = str(tmp_path / "h.db")
+    conn = sqlite3.connect(path, isolation_level=None)
+    conn.execute(f"PRAGMA journal_mode={journal_mode}")
+    for i in range(300):
+        conn.execute(f"create table t{i} (id integer)")
+    conn.execute("alter table t1 add column b")
+    version = conn.execute("PRAGMA schema_version").fetchone()[0]
+    if journal_mode == "wal":
+        # Pages still in the -wal: the main file header is stale, which is
+        # why the watcher only reads it when the -wal is empty
+        assert schema_watcher_module.fingerprint(path)[1] is not None
+        conn.execute("PRAGMA wal_checkpoint(TRUNCATE)")
+    assert schema_watcher_module.fingerprint(path)[1:] == (None, None)
+    assert schema_watcher_module.header_schema_version(path) == version == 301
+    conn.close()
+    assert (
+        schema_watcher_module.header_schema_version(str(tmp_path / "nope.db")) is None
+    )
+    (tmp_path / "junk.db").write_bytes(b"not a database" * 20)
+    assert (
+        schema_watcher_module.header_schema_version(str(tmp_path / "junk.db")) is None
+    )
+
+
 @pytest.mark.asyncio
+@pytest.mark.parametrize("use_header", (True, False))
 @pytest.mark.parametrize("racy_rule", (True, False))
-async def test_racily_clean_same_tick_change(db_path, monkeypatch, racy_rule):
+async def test_racily_clean_same_tick_change(
+    db_path, monkeypatch, racy_rule, use_header
+):
     """Two schema changes inside one timestamp tick, same file size and
     inode: only the racy-clean rule catches the second one."""
+    monkeypatch.setattr(schema_watcher_module, "USE_HEADER_CHECK", use_header)
     monkeypatch.setattr(
         schema_watcher_module,
         "fingerprint",