He starred in "Chucky Jack", an outdoor drama about Tennessee Governor John Sevier, at the old Hunter Hills Theater in Gatlinburg.

The original cast album received a Grammy Award (presented to lyricist Alan Jay Lerner and composer Burton Lane).

He also played the role at Wolf Trap, Virginia, in June 1976,[17] opened the national tour for 3 weeks in Fall 1977 in Chicago,[18] and starred in the limited run Broadway revival in 1989.

He followed Shenandoah by playing the maniacal Broadway producer Oscar Jaffee in the 1978 musical On the Twentieth Century, opposite Madeline Kahn and later Judy Kaye, earning his second Tony Award.

He received his fourth Tony nomination in 2002 for originating the role of evil moneygrubber corporate president Caldwell B. Cladwell in Urinetown The Musical.

Later Broadway appearances include the title role of William Shakespeare's seldom-performed Cymbeline, at Lincoln Center in 2007[19] and August: Osage County, by Tracy Letts for the week of September 16, 2008, and then since November 11, 2008.

[20] In addition to enjoying a long stage career, he is well known to television audiences for his regular role as Holling Vincoeur on the quirky CBS series Northern Exposure, his extended appearances on the NBC medical drama ER as Mark Greene's father, and on Law & Order: Special Victims Unit as constitutional lawyer and later judge, Barry Moredock.

John Cullum appeared on Broadway in The Scottsboro Boys (2010), a musical by Kander and Ebb about a notorious miscarriage of justice in the American South in the 1930s.