Following a string of unsuccessful plays, and with many actors moving out West, Watkin moved to California in 1935 to pursue a film career. He made his debut that same year in the Bette Davis film "Dangerous", which would be the beginning of a 25-year career. Watkin often appeared in bit roles — many uncredited — as distinguished authority figures. Many of Watkin's more prominent roles came from low-budget poverty row studios, and serials. His first serial came when he starred as the main antagonist in the Universal film serial "The Green Hornet Strikes Again!", his first film serial. Watkin would come to appear in prominent roles in several serials; in 1947, Watkin portrayed the role of Uncle Jim Fairfield in the Columbia serial "Jack Armstrong". Following this, Columbia cast him as Perry White in their "Superman" serial. The serial was the first adaption of the character, and was a success. Watkin would reprise his role in a follow-up, "Atom Man vs. Superman", in 1950. He also appeared in several Western films for Republic Pictures.