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Pullman made his film debut in Ruthless People (1986), and starred in Spaceballs (1987), The Accidental Tourist and The Serpent and the Rainbow (both 1988), Newsies (1992), Sleepless in Seattle (1993), Wyatt Earp (1994), While You Were Sleeping (1995), Independence Day (1996), Lost Highway (1997), and Lake Placid (1999). He also voiced Captain Joseph Korso in Titan A.E. (2000). He has also appeared frequently on television, usually in TV films. Since the 21st century began, Pullman has also acted in miniseries and regular series such as Torchwood (2011), playing starring roles in 1600 Penn (2012–13) and The Sinner (2017–2021). In 2021, he had a recurring role in the miniseries Halston.

Pullman also has a long stage-acting career. He has appeared on Broadway several times, including in Edward Albee's The Goat or Who Is Sylvia? (2002).