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Dunst first gained recognition for her role as child vampire Claudia in the horror film Interview with the Vampire (1994), which earned her a Golden Globe nomination for Best Supporting Actress. She also had roles in her youth in Little Women (1994) and Jumanji (1995). Dunst transitioned to leading roles in teen films of 1999, the satires Dick and Drop Dead Gorgeous and Sofia Coppola's drama The Virgin Suicides. After the leading role in the cheerleading film Bring It On (2000), she gained wider attention for her role as Mary Jane Watson in Sam Raimi's Spider-Man trilogy (2002–2007). Her career progressed with a supporting role in Eternal Sunshine of the Spotless Mind (2004), followed by a lead role in Cameron Crowe's tragicomedy Elizabethtown (2005), and as Marie Antoinette in Coppola's Marie Antoinette (2006).

In 2011, Dunst starred as a depressed newlywed in Lars von Trier's drama Melancholia, which earned her the Cannes Film Festival Award for Best Actress. In 2015, she played Peggy Blumquist in the second season of the FX series Fargo, earning a Primetime Emmy Award nomination for the role. Dunst had a supporting role in the film Hidden Figures (2016), and leading roles in Coppola's The Beguiled (2017) and in the dark comedy series On Becoming a God in Central Florida (2019), for which she received a third Golden Globe nomination. Dunst earned her fourth nomination for a Golden Globe and first nomination for an Academy Award for her performance in the psychological drama The Power of the Dog (2021). In 2024, she led the dystopian thriller film Civil War.