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Staunton has performed in a variety of plays and musicals in London throughout her career, winning four Laurence Olivier Awards; three for Best Actress in a Leading Role in a Musical for her roles in the musicals Into the Woods, Sweeney Todd, and Gypsy, and one for Best Performance in a Supporting Role in a Play for her work in both A Chorus of Disapproval and The Corn is Green. Her other stage appearances include The Beggar's Opera, The Wizard of Oz, Uncle Vanya, Guys and Dolls, Entertaining Mr Sloane, and Good People. She has been nominated for 13 Olivier Awards.

On film, Staunton starred in Antonia and Jane; in several supporting roles in Kenneth Branagh's comedy Peter's Friends, his adaptation of Much Ado About Nothing; Ang Lee's adaptation of Sense and Sensibility; and the costume romantic comedy Shakespeare in Love. She drew critical acclaim for her performance in the title role in Mike Leigh's Vera Drake, for which she won the BAFTA Award for Best Actress in a Leading Role and the Venice Film Festival Volpi Cup for Best Actress, in addition to being nominated for Best Actress by the Academy Awards, the Golden Globe Awards and the Screen Actors Guild Awards. She later gained a wider audience for her portrayal as Dolores Umbridge in the Harry Potter films The Order of the Phoenix and The Deathly Hallows - Part 1. She continued supporting roles in Nanny McPhee, reunited with Leigh in Another Year, and the film continuation of Downton Abbey. She portrayed human rights activist Hefina Headon in the historical film Pride, and starred in the British comedy Finding Your Feet. She also provided voice acting roles for the films Chicken Run, Arthur Christmas, and Paddington.

On television, Staunton starred in the sitcoms Up the Garden Path and Is it Legal?. Her performance in My Family and Other Animals earned her a nomination for the International Emmy Award for Best Actress, while her roles in Return to Cranford and The Girl earned her BAFTA TV Award nominations for Best Actress in a Supporting Role. For the latter, she was also nominated for the Primetime Emmy Award for Outstanding Supporting Actress in a Miniseries or a Movie. She portrayed Queen Elizabeth II in the final two seasons of The Crown.