His Broadway career included 15 productions, with notable appearances in Company, Cabaret, Zorba, 1776, Titanic, The Sisters Rosensweig, and Six Degrees of Separation. He originated the role of Flan Kittredge in Six Degrees of Separation on Broadway from 1990 to 1992 and later reprised it in the 1993 film adaptation.
Though theater was his artistic home, Cunningham was widely recognized on screen as the reserved father in Mystic Pizza and the stern yet caring parent in Dead Poets Society. His film credits also included School Ties, Nixon, The Jackal, Shaft, and Roommates, along with memorable voice work in In & Out and Starship Troopers. Television audiences saw him repeatedly over decades, including eight appearances on Law & Order, as well as roles on 30 Rock, The Good Wife, and Damages.

Born in 1932, Cunningham served in the U.S. Army before earning a master’s degree from Yale Drama School. He remained active in arts education and community work throughout his life. He is survived by his wife of nearly 70 years, Carolyn Cunningham, their children, grandchildren, and great-grandchildren. John Cunningham leaves behind a legacy of quiet excellence, professionalism, and enduring respect.