Along with John Carradine, Donald Meek, Ward Bond, Ben Johnson, Harry Carey, Jr. et al., Whitehead was one of the many actors regularly employed by Ford to breathe life into even the smallest roles in his films.

Whitehead's film debut was in The Scoundrel (1935) by Ben Hecht, and Charles MacArthur which won a 1936 Oscar for Best Original Story[4] Whitehead most famously played Al Joad (Henry Fonda's younger brother) in John Steinbeck's Grapes of Wrath (1940) which was nominated for, and won, several Oscars.

[5] Whitehead starred as Clarence in a stage production of Life with Father with Lillian Gish[6] among a total of more than 50 films and TV series episodes performances.

In 1966 he won the Best Supporting Actor award at the Dublin Theatre Festival for his performance in Eugene O'Neill's Hughie, a part he was to reprise at the Peacock until 1989.

In 1983 he played the role of American Ambassador David Gray in the RTÉ television drama Caught in a Free State, set in neutral Ireland during World War II.

Z. Whitehead Award" supporting theatre in 1966,[1] the first year including Dr. Michael McDonnell,[7] for his play All Gods Die on Friday.