After a number of films, Drake co-starred with Judy Garland in Meet Me in St. Louis (1944) as John Truett, the boy next door. He appeared in more than forty films in all, including Mrs. Parkington (1944), The Green Years (1946), Cass Timberlane (1947), as Composer Richard Rodgers in the loosely-based biography Words and Music (1948) and, in a role at the opposite end of the character spectrum from John Truett, as the leader of a gang of Criminals in Warlock (1959). He also had a minor role in the movie The Singing Nun (1966), playing Ed Sullivan's Producer Mr. Fitzpatrick.