Dunst achieved fame for her portrayal of Mary Jane Watson in Sam Raimi's Spider-Man trilogy (2002–2007). Since then, her films have included the romantic comedy Wimbledon (2004), the science fiction romantic comedy-drama Eternal Sunshine of the Spotless Mind (2004) and Cameron Crowe's romantic tragicomedy Elizabethtown (2005). She played the title role in Sofia Coppola's biographical film Marie Antoinette (2006) and starred in the comedy film How to Lose Friends & Alienate People (2008). She won the Best Actress Award at the Cannes Film Festival and the Saturn Award for Best Actress for her performance in Lars von Trier's Melancholia (2011). She starred in the second season of the television series Fargo in 2015, playing the role of Peggy Blumquist, a hairdresser who gets mixed up in a war between two crime families. Her performance garnered widespread critical acclaim, leading to her winning the Critics' Choice Television Award for Best Actress and being nominated for the Golden Globe Award for Best Actress and the Primetime Emmy Award for Outstanding Lead Actress in a Limited Series or Movie, losing to Lady Gaga and Sarah Paulson, respectively.
In 2017, Dunst won her first Screen Actors Guild Award for her performance in the drama Hidden Figures (2017), about women mathematicians in the space program, and co-starred in her third collaboration with Sofia Coppola, the historical drama thriller The Beguiled.
In 2001, Dunst made her singing debut in the film Get Over It, in which she performed two songs. She also sang the jazz song "After You've Gone" for the end credits of the film The Cat's Meow (2001).