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Wilton is known for starring opposite Richard Briers in the BBC sitcom Ever Decreasing Circles (1984–1989), playing Homily in The Borrowers (1992) and The Return of the Borrowers(1993), and for her role as the widowed Isobel Crawley in the ITV drama Downton Abbey (2010–2015). She also played the recurring role of Harriet Jones in Doctor Who (2005–2008) and Anne in Ricky Gervais' Netflix dark comedy After Life.

Wilton has had an extensive career on stage, receiving six Olivier Award nominations. She was nominated for Man and Superman (1981), The Secret Rapture (1988), The Deep Blue Sea(1994), John Gabriel Borkman (2008) and The Chalk Garden (2009) before winning the 2015 Olivier Award for Best Actress for Taken at Midnight. Her film appearances include Clockwise (1986), Cry Freedom (1987), Blame It on the Bellboy (1992), Calendar Girls (2003), Shaun of the Dead (2004), Match Point (2005), Pride & Prejudice (2005), The Best Exotic Marigold Hotel (2012), The Girl (2012), The BFG (2016) and The Unlikely Pilgrimage of Harold Fry (2023).