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Born to actors Eric Thompson and Phyllida Law, Thompson was educated at Newnham College, Cambridge, where she became a member of the Footlights troupe and appeared in the comedy sketch series Alfresco (1983–1984). In 1985, she starred in the West End revival of the musical Me and My Girl, which was a breakthrough in her career. In 1987, she became famous for her performances in two BBC series, Tutti Frutti and Fortunes of War, winning the BAFTA TV Award for Best Actress for her work on both series. In the early 1990s, she often collaborated with then-husband, actor and director Kenneth Branagh in films such as Henry V (1989), Dead Again (1991), and Much Ado About Nothing (1993).

Thompson won the BAFTA Award and the Academy Award for Best Actress for her performance in the Merchant-Ivory period drama Howards End (1992). In 1993, she received two Academy Award nominations—Best Actress and Best Supporting Actress—for the respective roles of the housekeeper of a grand household in The Remains of the Day and a lawyer in In the Name of the Father, becoming one of the few actors to achieve this feat. Thompson wrote and starred in Sense and Sensibility (1995), for which she won the Academy Award for Best Adapted Screenplay—making her the only person in history to win Oscars for both acting and writing—and once again won the BAFTA. Further critical acclaim came for her roles in Primary Colors (1998), Love Actually (2003), Saving Mr. Banks (2013), Late Night (2019), and Good Luck to You, Leo Grande (2022).

Other notable film credits include the Harry Potter series (2004–2011), Nanny McPhee (2005), Stranger than Fiction (2006), An Education (2009), Men in Black 3 (2012) and the spin-off Men in Black: International (2019), Brave (2012), Beauty and the Beast (2017), Cruella (2021), and Matilda the Musical (2022). Her television credits include Wit (2001), Angels in America (2003), The Song of Lunch (2010), King Lear (2018) and Years and Years (2019). She portrayed Mrs. Lovett in a Lincoln Center production of Stephen Sondheim's Sweeney Todd: The Demon Barber of Fleet Street in 2014. Authorised by the publishers of Beatrix Potter, Thompson has also written three Peter Rabbit children's books.