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He has starred in such films as The Thing (1982), Platoon (1986), They Live (1988), Dead Presidents(1995), Armageddon (1998), There's Something About Mary (1998), Requiem for a Dream (2000), Pitch Black (2000), Barbershop (2002), Crash (2004), The Chronicles of Riddick (2004), Cloud Atlas (2012), The Nice Guys (2016), Nope (2022), and American Fiction (2023). He starred as Elroy Patashnik in the sixth season of the NBC series Community (2015) and as Bishop James Greenleaf in the Oprah Winfrey Network drama Greenleaf (2016–2020).

His Emmy-winning voice acting career includes narrating Ken Burns films such as The War (2007) and Muhammad Ali (2021). In film, he has voiced Dr. Facilier in The Princess and the Frog (2009) and the Cat in Coraline (2009). On television, he portrayed Goliath in Gargoyles (1994–1997), Al Simmons / Spawn in Todd McFarlane's Spawn (1997–1999), The Flame King in Adventure Time (2012–2017), President Andre Curtis in Rick and Morty (2015–) and its upcoming spin-off President Curtis, King Andrias in Amphibia (2020–2022), Dr. Tenma in Pluto (2023), and Husk in Hazbin Hotel (2024–). Video game roles include the Arbiter Thel 'Vadamee in the Halo franchise (2004–2015), Julius Little and himself in the Saints Row series (2006–2017), Captain Anderson in the Mass Effect series (2007–2013), Chaos in Dissidia Final Fantasy (2008), Sergeant Foley in Call of Duty: Modern Warfare 2 (2009), and Commander Zavala in Destiny 2: The Final Shape (2024), which he assumed after the death of Lance Reddick in March 2023. He was part of the cast of The Nightmare Before Christmas live concert in October 2025, where he voiced Oogie Boogie, taking over the role from his longtime original voice actor, Ken Page, following his death in September 2024.

In July 2025, David was selected to receive a star on the Hollywood Walk of Fame in 2026.