She also sang the jazz song "After You've Gone" for the end credits of the film The Cat's Meow (2001).
In 1993, her parents separated, and she subsequently moved with her mother and brother to Los Angeles, where she attended Laurel Hall School in North Hollywood and Notre Dame High School.
Derek Elley of Variety described the film as "playful and sporty", saying that this was Dunst's best performance to date: "Believable as both a spoiled ingenue and a lover to two very different men, Dunst endows a potentially lightweight character with considerable depth and sympathy." In 2002, Dunst co-starred opposite Tobey Maguire in the superhero film Spider-Man, the most financially successful film of her career to date.
She played Mary Jane Watson, the best friend and love interest of Peter Parker (Maguire). Owen Gleiberman of Entertainment Weekly remarked on Dunst's ability to "lend even the smallest line a tickle of flirtatious music." In the Los Angeles Times review, critic Kenneth Turan noted that Dunst and Maguire made a real connection on screen, concluding that their relationship "involved audiences to an extent rarely seen in films." Also in 2004, Dunst co-starred opposite Paul Bettany in the romantic comedy Wimbledon where she portrayed a rising tennis player in the Wimbledon Championships, while Bettany portrayed a fading former tennis star.
In 2015, Dunst co-starred as Peggy Blumquist in the second season of the critically acclaimed FX crime comedy-drama Fargo, for which she received a Golden Globe nomination.
She later explained: "When I read it, I was 15 and I don't think I was mature enough to understand the script's material." That same year, she co-starred in the comedy film Dick, opposite Michelle Williams. Dunst co-starred opposite James Woods in Sofia Coppola's drama film The Virgin Suicides (1999), based on Jeffrey Eugenides' novel of the same name.
Dunst starred as the magical princess Majokko in the Takashi Murakami and Mc G directed short Akihabara Majokko Princess singing a cover of The Vapors' 1980 song "Turning Japanese".
This was shown at the "Pop Life" exhibition in London's Tate Modern museum from October 1, 2009, to January 17, 2010.
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.