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Born and raised in Cleveland, Henton never entertained the thought of a career in comedy. In 1982, while working during the day and studying computer science at night, he was urged by a co-worker to try his jokes at a local comedy club's amateur night. By his second night, he won the amateur night contest and began stand-up part-time. Henton made the move to Los Angeles in 1985 and by 1988 started his stand-up career full-time.

After taking his comedy on the road for a year and winning the 1991 Johnny Walker National Comedy Search, Henton was spotted by a The Tonight Show with Johnny Carson comedy executive who booked him for a performance on the show. As he finished his set, Henton looked to Carson for his approval and received much more. Henton was called over to take a seat on the coveted couch where Carson asked him if he had an agent. To Henton's reply of no, Carson mugged, Well, you will after tonight. It was a performance that Henton says gave his career a "serious jump-start.

Since then Henton has made appearances on many television programs, starred in his own half-hour comedy special for Showtime, John Henton: Comedy With an Attitude and was cast in the TV series Living Single with Queen Latifah and Kim Fields Freeman. The show received stellar ratings and TV Guide selected Henton's character as one of the break-out characters of the season.

Although Henton lives in Los Angeles, he will always call Cleveland home. Currently, he is still learning to play golf.