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As a child in Arizona, Stone started acting in local theatre productions before relocating to Los Angeles to pursue a career in the film industry. As a teenager, she made her television debut in the reality show In Search of the New Partridge Family (2004). After small television roles, she appeared in a string of successful comedy films, including Superbad (2007), Zombieland (2009), and Easy A (2010), which marked Stone's first leading role. Following this breakthrough, she starred in the romantic comedy Crazy, Stupid, Love (2011) and the period drama The Help (2011). She gained wider recognition as Gwen Stacy in Marc Webb's Spider-Man films (2012–2014).

Stone cemented her status as a leading lady by taking on more eclectic and dramatic roles. She earned nominations for the Academy Award for Best Supporting Actress for portraying a recovering drug addict in the surrealist dark comedy Birdman (2014) and Abigail Hill in the absurdist period film The Favourite (2018); the latter marked her first of many collaborations with Yorgos Lanthimos. She won two Academy Awards for Best Actress for portraying an aspiring actress in the romantic musical La La Land (2016) and a resurrected suicide victim in Lanthimos's Poor Things (2023); she was also nominated for the Academy Award for Best Picture for the latter. Stone also earned recognition for portraying tennis player Billie Jean King in Battle of the Sexes (2017) and the titular role in Cruella (2021). She has since collaborated twice more with Lanthimos, starring in the anthology film Kinds of Kindness (2024) and the dark comedy Bugonia (2025); the latter earned her further nominations for the Academy Award for Best Actress and Best Picture, making her the first woman to be nominated as both a producer and an actress in two different films.

On Broadway, Stone starred as Sally Bowles in a revival of the musical Cabaret (2014–2015). On television, she has led the dark comedy miniseries Maniac (2018) and The Curse (2023). She and her husband, Dave McCary, founded the production company Fruit Tree in 2020.