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Thewlis made his film debut in Little Dorrit (1987) and acted in the Mike Leigh films Life is Sweet (1990) and Naked (1993), winning the Cannes Film Festival Award for Best Actor for the latter. He then appeared in films such as Black Beauty (1994), Restoration (1995), James and the Giant Peach (1996), Dragonheart (1996), and Seven Years in Tibet (1997). He became more widely known to film audiences for his roles as Remus Lupin in the Harry Potter franchise (2004–2011) and Ares / Sir Patrick Morgan in Wonder Woman (2017). Other film roles include Kingdom of Heaven (2005), The Boy in the Striped Pyjamas (2008), War Horse (2011), The Theory of Everything (2014), Anomalisa (2015), I'm Thinking of Ending Things (2020), and Enola Holmes 2 (2022).

Thewlis' most notable television roles include V. M. Varga in the third season of FX's Fargo (2017), the voice of the Shame Wizard in the Netflix animated sitcoms Big Mouth (2017–present) and Human Resources (2022–present), Christopher Edwards in the HBO miniseries Landscapers (2021), and John Dee in the Netflix drama series The Sandman (2022). His performance in Fargo earned him nominations for an Emmy, a Golden Globe, and a Critics' Choice Award.