Sullivan appeared mostly in television roles during his career. In the mid-1950s, he appeared on the religion anthology series, Crossroads. Sullivan and Angie Dickinson appeared together in the episode "Point of Honor" of the syndicated American Civil War drama series, The Gray Ghost. He guest starred as Jason Douglas in the 1960 episode "The Target" of the syndicated western series Tombstone Territory.

In 1961-62, Sullivan made three guest appearances on Perry Mason, including the 1962 episode "The Case of the Unsuitable Uncle" and in each episode played the murder victim. He portrayed Patrick Henry in the Daniel Boone episode "Love and Equity", scientist Anthony Sterling in the Voyage to the Bottom of the Sea episode "Leviathan", Nexus in the Lost in Space episode "His Majesty Smith", an Army Lieutenant in the episode "The Winter Soldier" on Rawhide, Mr. Willis in Knots Landing, Dr. Burt Hammond in St. Elsewhere, and Mr. Plenn in Falcon Crest.

In 1966–67 season, he appeared as Major Mapoy in all twenty-six episodes of the ABC Western series The Monroes with Michael Anderson, Jr., and Barbara Hershey. He appeared in films such as That Darn Cat! (1965) as Graham and The Magic Sword (1962). Sullivan performed the role of Parmen, a supremely arrogant and cruel telekinetic alien, in the Star Trek episode "Plato's Stepchildren" (1968). He was also featured in the Twilight Zone episodes "The Changing of the Guard" and "The Silence". In the latter episode, which aired in 1961, he played a youngish and overly loquacious member of a gentleman's club who accepts a challenging and rather bizarre bet offered by an older member of the club (played by actor Franchot Tone) which ends in unintended, classic Twilight Zone consequences. In the former episode, which aired a year later in 1962, Sullivan played the Headmaster of a private boarding school who must deliver the bad news to an "aging out" Teacher, played by Donald Pleasence.

He played the prosecuting attorney in the Hill 256 Episode of Combat!. In the Dragnet episode "The Big Prophet" (1968) Sullivan gave a tour de force performance as his character, "Brother William" (a thinly disguised portrayal of Timothy Leary) held forth for the entire half-hour on the benefits of LSD and marijuana, while Joe Friday argued the opposing view.

Telepathy was the subject of experiments Sullivan conducted in the documentary film from 1977 called The Amazing World of Psychic Phenomena hosted by Raymond Burr. Sullivan often portrayed villains throughout his acting career. He once said, "Playing truly evil people is a great way to release tension and anger and disgust with humanity. Show bad people what they really look and act like and maybe they'll recognize themselves and change. Who knows?"

Sulivan died Sunday, April 19, 1998 in Los Angeles of a heart attack at the age of 74. He had recently completed a role in Mike Nichols's production of The Little Foxes. At the time of his death, Sullivan was working on two books: a novel and the history of his family's Eli Bridge Co., which was credited with constructing one of the first Ferris wheels. He was interred at Diamond Grove Cemetery in his native Jacksonville, Illinois.