Naughton graduated from Brown University and Yale Drama School. His acting career began when he appeared in a series of Broadway dramas and musicals. He has since become an accomplished actor in both starring and supporting film and television roles.

His largest fame and first love has been the legitimate theater. He won the Theatre World Award for his performance in Long Day's Journey Into Night in 1971. He went on to star with Genevive Bujold in Antigone which was later made into a film in 1974. He starred in the musical I Love My Wife in 1977 and in the drama Whose Life is it Anyway? opposite Mary Tyler Moore in 1980. He won his first Tony Award for Best Actor in a Musical in 1990 for City of Angels. In 1997 he won a second Tony Award with his portrayal of lawyer Billy Flynn in the musical Chicago.

He created the lead role of Willy Brandt, Chancellor of West Germany, in the highly acclaimed drama Democracy in 2004.

His films include The Paper Chase and The First Wives Club. In 2006, he appeared in the movie The Devil Wears Prada, opposite Meryl Streep. In 2006, he played the part of Edie Sedgwick's father, Fuzzy Sedgwick in Factory Girl.

On television, he starred in Faraday & Company with Dan Daily and Sharon Gless (19731974). He also starred with Ron Harper in the 1974 television series cult-classic Planet of the Apes, a spin-off of the original movie. He starred in Making the Grade and Trauma Center in the early 1980s. He starred in the short lived series Raising Miranda in 1988. He co-starred with Bill Cosby in The Cosby Mysteries in 1995. He has also done numerous guest-star roles on television, including several different villains on Law & Order produced by his Brown University classmate, Jeffrey L. Hayes.

He appeared with Sharon Gless twenty years later, this time as her husband in Cagney and Lacey: the Return (1993) and Cagney and Lacey:Together Again (1995). More recently, he appeared on Damages with Glenn Close. He has appeared in television commercials promoting the drugs Cialis, Nexium and Nasalcrom. Mr. Naughton has also been the official voice of Audi in the U.S. since 2007. His voice can be heard in their national TV and Radio spots. He is also a frequent narrator on PBS television's Nature series.

He has directed several plays in New York, including the 2002 revival of Thornton Wilder's Our Town, starring his close personal friend Paul Newman, which was filmed for cable TV in 2003. He also appears in cabarets in New York City, including Manhattan Theater Club and Caroline's Comedy Club.

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