Outside of the theatre world, Cullum is best known for his role as tavern owner Holling Vincoeur in the television drama series Northern Exposure, for which he was nominated for an Emmy Award for Best Supporting Actor in a Drama. He was featured in fifteen episodes of the NBC television series ER as Dr. Mark Greene's father. He played farmer Jim Dahlberg in the landmark television drama The Day After. He made multiple guest appearances on Law & Order and Law & Order: Special Victims Unit as attorney/judge Barry Moredock, and appeared as Big Mike in several episodes of The Middle. He appeared as Senator Beau Carpenter on the CBS series Madam Secretary.
Cullum was married to Emily Frankel from 1959 until her death in 2024.[citation needed] They have one son, JD Cullum (John David Cullum), who is also an actor.[10]
In 1965, he was called in to replace Louis Jourdan during the Boston tryout of the musical On a Clear Day You Can See Forever.[14] It was his first starring role on Broadway, netting him a Theatre World Award and his first Tony Award nomination. The original cast album received a Grammy Award (presented to lyricist Alan Jay Lerner and composer Burton Lane).
He portrayed Edward Rutledge of South Carolina in the Broadway musical 1776, providing a dramatic highlight with his performance of "Molasses to Rum," a tirade against the hypocrisy of some Northerners over the slave trade ("They don't keep slaves, but they are willing to be considerable carriers of slaves to others. They're willing – for the shilling.") Cullum had been the third Rutledge on Broadway,[15] but played the role the longest and repeated it for the 1972 film.
He is well known for premiering the role of Charlie Anderson in the musical Shenandoah, which began at Goodspeed Opera House, Connecticut in 1974.[16] Cullum won the Tony, Drama Desk and Outer Critics Circle Awards when the show was produced on Broadway in 1975. 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.[14] He earned his fifth Tony nomination in the 2007 revival of 110 in the Shade, playing H.C. Curry, father to Audra McDonald's Lizzie.
In 2003, Cullum co-starred with Northern Exposure castmate Barry Corbin in Blackwater Elegy, a short film written by Matthew Porter and co-directed by Porter and Joe O'Brien.
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. Cullum has also appeared as Lucky Strike executive Lee Garner, Sr. on AMC's Mad Men. He appeared as Leap Day William, the embodiment of the fictional Leap Day national holiday, in the "Leap Day" episode of the sixth season of NBC's 30 Rock.
John Cullum was inducted into the Theatre Hall of Fame in 2007.[21]
In 2015 Cullum appeared and sang in the satirical B&W period movie-musical footage of Daddy's Boy on Unbreakable Kimmy Schmidt. The "forgotten footage" features comically incestuous lyrics set in an innocent context that apes classic 1930's films.[22]
Cullum, then an octogenarian, joined the cast of Waitress as Joe on October 12, 2017, replacing Larry Marshall.[23]