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Lithgow won two Tony Awards, his first for Best Featured Actor in a Play for his Broadway debut in The Changing Room (1972) and his second for Best Actor in a Musical for the musical Sweet Smell of Success (2002). He was Tony-nominated for Requiem for a Heavyweight (1985), M. Butterfly (1988), and Dirty Rotten Scoundrels (2005). He has acted in the plays The Columnist (2012), A Delicate Balance (2014), and Hillary and Clinton (2019). He portrayed Roald Dahl in the play Giant on the West End, for which he was nominated for the Olivier Award for Best Actor.

He starred as Dick Solomon in the television sitcom 3rd Rock from the Sun (1996–2001), winning three Primetime Emmy Awards for Best Actor in a Comedy Series. He received further Primetime Emmy Awards for his performances as Arthur Mitchell in the drama Dexter (2009) and as Winston Churchill in the Netflix drama The Crown (2016–2019). He also starred in HBO's Perry Mason (2020) and FX's The Old Man (2022).

On film, he has received two Academy Awards for Best Supporting Actor nominations for his roles as a transgender ex-football player in The World According to Garp (1982) and a lonely banker in Terms of Endearment (1983). He also acted in All That Jazz (1979), Blow Out (1981), Footloose (1984), Harry and the Hendersons (1987), A Civil Action (1998), Shrek (2001), Kinsey (2004), Rise of the Planet of the Apes (2011), Love Is Strange (2014), Interstellar (2014), Late Night (2019), Bombshell (2019), Killers of the Flower Moon (2023), and Conclave (2024).