Dunst was born in Point Pleasant, New Jersey, to Inez and Klaus Dunst, who are separated. Her father, a German medical services executive from Hamburg, remained in New Jersey. Her mother, a Swedish former art gallery owner, moved to California. Dunst has a younger brother, Christian.
Dunst attended the Ranney School in New Jersey, but graduated in 2000 from Notre Dame High School in the Sherman Oaks neighborhood of Los Angeles, California.
Dunst got her start as a child fashion model at the age of three in television commercials. She was signed with Ford Models and Elite Model Management. In a 1988 episode of Saturday Night Live, she played the role of President George H. W. Bush's granddaughter, in a sketch in which Dana Carvey acted as President Bush. In 1989, Dunst moved to the big screen with New York Stories. Soon after, she landed a small part in The Bonfire of the Vanities as Tom Hanks's daughter. Dunst also did the voice of Kiki in the 1989 anime film Kiki's Delivery Service. In 1993, Dunst played Hedril in the seventh season episode of Star Trek: The Next Generation called "Dark Page". She also had a recurring role as a child prostitute, Charlie Chiemingo, on ER.
Her feature film breakthrough came in Interview with the Vampire, a 1994 film based on Anne Rice's novel. The movie featured a scene in which Dunst, then-aged eleven, kissed Brad Pitt, who was 29. Her performance earned her a Golden Globe nomination, the MTV Award for Best Breakthrough Performance and the Saturn award for Best Young Actress. In 1995, she was named one of People Magazine's 50 Most Beautiful People. Dunst was also offered the role of Angela in the 1999 Academy Award-winning film American Beauty, but turned it down because she did not want to appear in the film's suggestive sexual scenes or kiss co-star Kevin Spacey. The same year, she had the role of troubled adolescent Lux Lisbon in Sofia Coppola's Independent film The Virgin Suicides. In June of 2000 she graduated from Notre Dame High School in Los Angeles.
At the 2002 Mar de Plata Film Festival, Dunst won the Best Actress Silver OmbÃº for her performance as Charlie Chaplin's love interest Marion Davies in Peter Bogdanovich's The Cat's Meow. Dunst made her singing debut in the 2001 film Get Over It, performing two songs written by Marc Shaiman. Previously had appeared in the music video for Savage Garden's "I Knew I Loved You". She also lent her musical voice to the end credits of The Cat's Meow by singing the old standard, "After You've Gone."
Dunst's most recent film is Marie Antoinette, which premiered at the 2006 Cannes Film Festival and was released in North America on October 20, 2006. In the film, her second with director Sofia Coppola, Dunst plays the title character and uses an American accent in the role.
Dunst is slated to portray peace activist Marla Ruzicka in Sweet Relief scripted by Lorene Scafaria for Warner Independent Pictures in 2009. Dunst also reprises her role of Mary Jane Watson in Spider-Man 3, which is scheduled for a release on May 4, 2007. Dunst initially signed on to appear in three Spider-Man films, and has said that she would not appear in a fourth film unless director Sam Raimi returned to direct. In another project, she is rumored to play Blondie frontwoman Deborah Harry in director Michel Gondry's upcoming biopic about the band.
Dunst recently stated in an interview in 2006 while promoting Marie Antoinette that she wants to take a break from appearing in films to study and pursue art.
She started dating actor Jake Gyllenhaal in September 2002, after meeting him through his sister, Maggie Gyllenhaal (her Mona Lisa Smile co-star). They officially broke up in July 2004 but remained off and on until December 2005. They adopted a dog together, called "Atticus". She has recently been seen with Indie British rocker Johnny Borrell, at the South by Southwest Music Festival in Austin, Texas.