In 2009, she appeared in a new production of Endgame by Samuel Beckett at the Duchess Theatre in the West End. She was one of the original cast of the London production of the musical Wicked opposite Idina Menzel in 2006, playing Madame Morrible, a role she played again on Broadway in 2008. In 2004, Margolyes played the role of Peg Sellers, the mother of Peter Sellers, in the Golden Globe winning film The Life and Death of Peter Sellers. In a 2011 interview on The Graham Norton Show, in regard to her Potter costars, Margolyes said that she got on well with Maggie Smith, but rather bluntly admitted that she, "didn't like the one that died", referring to Richard Harris. She reprised her role as Professor Sprout in Harry Potter and the Deathly Hallows – Part 2 (2011). She played Professor Sprout in Harry Potter and the Chamber of Secrets released in 2002. She voiced the rabbit character in the animated commercials for Cadbury's Caramel bars and provided the voice of Fly the dog in the Australian-American family film Babe (1995). She played the Nurse in Baz Luhrmann's Romeo + Juliet (1996). Margolyes played Aunt Sponge and voiced the Glow-Worm in James and the Giant Peach (1996). In 1989, Margolyes co-wrote and performed a one-woman show, Dickens' Women, in which she played 23 characters from Dickens' novels. In 1994, she won the BAFTA Award for Best Supporting Actress for her role as Mrs Mingott in Martin Scorsese's The Age of Innocence (1993). On American television, she headlined the short-lived 1992 CBS sitcom Frannie's Turn. She won the 1989 LA Critics Circle Award for Best Supporting Actress for her portrayal of Flora Finching in the film Little Dorrit (1988). In 1986, she played a major supporting role in the BBC drama The Life and Loves of a She-Devil. In the 1980s, she made appearances in Blackadder opposite Rowan Atkinson: these roles include the Spanish Infanta in The Black Adder, Lady Whiteadder in Blackadder II and Queen Victoria in Blackadder's Christmas Carol. Margolyes' first major role in a film was as Elephant Ethel in Stand Up, Virgin Soldiers (1977).
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In 1974, she appeared with Kenneth Williams and Ted Ray in the BBC Radio 2 comedy series The Betty Witherspoon Show.
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She also worked with the theatre company Gay Sweatshop and provided voiceovers in the Japanese TV series The Water Margin (credited as Mirium Margolyes). She performed most of the supporting female characters in the dubbed Japanese action TV series Monkey. In the 1970s, she recorded a soft-porn audio called Sexy Sonia: Leaves from my Schoolgirl Notebook. With her versatile voice, Margolyes first gained recognition for her work as a voice artist.
She represented Newnham College in the first series of University Challenge, where she may have been one of the first people to say " fuck" on British television she claims to have used the word in frustration on the show in 1963. There, in her 20s, she began acting and appeared in productions by the Cambridge Footlights. Margolyes attended Oxford High School and Newnham College, Cambridge, where she read English. Her grandfather Margolyes was born in a small shtetl called Amdur (now – Indura) in Belarus, which at that time was part of the Russian Empire. Her maternal great-grandfather, Symeon Sandmann, was born in the Polish town of Margonin, which Margolyes visited in 2013. She grew up in a Jewish family, with ancestors who moved to the UK from Belarus and Poland. Margolyes was born in Oxford on, the only child of Joseph Margolyes (1899–1995), a Scottish physician and general practitioner from the Gorbals area of Glasgow, and property-developer Ruth (née Walters 1905–1974), daughter of a second-hand furniture dealer and auctioneer at Kirkdale, Liverpool, who later relocated to London.