Dukes' film career included 35 movies. Throughout his career, he was a television guest star, notably as the man who attempted to rape Edith Bunker on All in the Family and as a blind bully on Three's Company. During the 1980s, Dukes appeared in the dual miniseries The Winds of War and War and Remembrance. He received an Emmy nomination for best supporting actor for his role in The Josephine Baker Story (1991) and appeared as Arthur Miller in Norma Jean & Marilyn (1996). He was a regular in the first season of Sisters, playing the transvestite husband of oldest sister, Alex (Swoosie Kurtz). Dukes' role became a recurring character in subsequent seasons. On Dawson's Creek, he had the recurring role of Mr. McPhee, father to Jack (Kerr Smith) and Andie (Meredith Monroe) from the second through fourth seasons. He also starred in Without A Trace as the ex-husband of Kate Nelligan.