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Spader began acting in youth-oriented films such as Tuff Turf, The New Kids (both 1985), Pretty in Pink (1986), and Mannequin (1987). His breakthrough role came with the Steven Soderbergh drama Sex, Lies, and Videotape (1989), for which he received the Cannes Film Festival Award for Best Actor. He then starred in films such as White Palace (1990), True Colors (1991), Stargate (1994), 2 Days in the Valley (1996), and Secretary (2002). Spader took supporting roles in Bob Roberts (1992), Wolf (1994), Lincoln (2012), and The Homesman (2014). He also played the role of Ultron in the Marvel Cinematic Universe film Avengers: Age of Ultron (2015).

His television roles include the attorney Alan Shore in the last season of The Practice (2003–2004) and its spin-off Boston Legal (2004–2008), which earned him three Primetime Emmy Awards for Outstanding Lead Actor in a Drama Series. He portrayed Robert California in the sitcom The Office (2011–2012). He then starred as Raymond Reddington in the NBC crime thriller series The Blacklist (2013–2023), for which he received two Golden Globe Award nominations for Best Actor – Television Series Drama.