Kerr's first television acting role was in 1954 on NBC's Justice as a basketball player who believes that gamblers have ruined his success on the court. His mother appeared with him on the series, which focuses on the cases of attorneys with the Legal Aid Society of New York.
He co-starred with Leslie Caron in Gaby (1956), the third remake of Waterloo Bridge, which, in its original pre-Code 1931 version, featured John's grandfather, actor Frederick Kerr. John Kerr starred with Deborah Kerr (no relation) in Tea and Sympathy (1956).
In a widely publicized decision in 1956, Kerr declined to play the role of Charles Lindbergh in The Spirit of St. Louis because he did not respect Lindbergh's early support of the Nazi regime in Germany prior to America's entry into World War II. "I don’t admire the ideals of the hero,” Mr. Kerr told The New York Post. The part went to James Stewart.
Kerr had a major role in the film version of Rodgers and Hammerstein's South Pacific (1958), playing Lt. Joe Cable, the newly arrived marine about to be sent on a dangerous spy mission. In The Crowded Sky (1960), Kerr played a pilot who helps the Captain (Dana Andrews) steer a crippled airliner back to earth. Another film appearance was in Roger Corman's The Pit and the Pendulum (1961). In 1963, Kerr had a continuing role on "Arrest and Trial", playing Assistant DA Barry Pine.
In 1965, Kerr guest starred on NBC's The Alfred Hitchcock Hour. He had a regular role on the ABC-TV primetime TV series, Peyton Place, playing District Attorney John Fowler during the 1965-66 season. In 1964-65 he appeared as guest star on several episodes of Twelve O'Clock High. During the 1970s, Kerr had a recurring role as prosecutor Gerald O'Brien on The Streets of San Francisco. Kerr's last appearance as an actor was a minor role in The Park Is Mine (1986), a made-for-TV movie starring Tommy Lee Jones.