Fanning started acting at the age of 2 years and 8 months. She began her acting career by playing the younger version of her older sister Dakota’s characters in both the mini-series Taken and the movie I Am Sam. In 2002, at the age of four, Fanning, in the comedy Daddy Day Care, won her first role independent of her sister.
In 2003, Fanning filmed The Door in the Floor opposite Jeff Bridges and Kim Basinger. Anecdotal evidence of her emerging skill was seen in the decision to cast her in the role of Ruth in The Door in the Floor. The film’s producers had originally planned to hire identical twins for the intense shooting schedule, but were so impressed with Fanning that they used only her.
Late in 2003, Fanning appeared in Because of Winn-Dixie in the small role of Sweetie Pie Thomas. In 2004, she did voicework in the English dubbed version of Miyazaki’s animated film My Neighbor Totoro, in the role of Mei. Later that same year, she filmed I Want Someone To Eat Cheese With. In early 2005, Fanning filmed scenes in Charlotte’s Web as the “future granddaughter” of Fern Arable played by Dakota Fanning. However, the scenes didn’t make the final cut. In mid 2005, she played Debbie, the daughter of Richard and Susan Jones (played by Brad Pitt and Cate Blanchett) in the Academy Award-winning film Babel. In early 2006, Fanning filmed scenes in both The Nines and Déjà Vu. In mid 2006, she filmed The Lost Room a sci-fi TV mini-series. Also in 2006, she appeared on the episode Need to Know of House, playing the patients daughter.
By the end of 2006, Fanning began to book lead roles. The first of these was the one of Emma Learner in Reservation Road—the grieving daughter of Grace and Ethan Learner. The film deals with the aftermath of a tragic car accident in that Emma’s brother is killed. Late in 2008, Fanning had a small part in The Curious Case of Benjamin Button as a younger version of Cate Blanchett’s character. Mid-year 2007, Fanning filmed the title role Phoebe of Phoebe in Wonderland—the fantastical tale of a little girl who won’t—or can’t—follow the rules. Phoebe in Wonderland also starred Felicity Huffman and was released in March 2009.
From July through October 2007, Fanning appeared in The Nutcracker in 3D, playing Mary. Set in 1920s Vienna, this is a tale of a little girl whose godfather gives her a special doll on Christmas Eve. The movie was filmed in Budapest, Hungary and was released late 2010.
In March 2008, Fanning and her sister Dakota were scheduled to star in My Sister’s Keeper, but the opportunity fell through when Dakota learned she would have to shave her head. The sisters were immediately replaced by Abigail Breslin and Sofia Vassilieva.
Variety reported in April 2009 that Fanning would be starring in Academy Award-winning screenwriter Sofia Coppola’s new film, Somewhere. The plot centers around a “bad-boy” actor who is forced to re-evaluate his life when his daughter, played by Fanning, arrives unexpectedly. The film was released during the 2010 awards season. At its first film festival, the 67th Venice Film Festival, it took out the Golden Lion.
Fanning starred in J. J. Abrams’ sci-fi film Super 8 as Alice Dainard. The movie was released on June 10, 2011 and centers around a group of kids who are forced to deal with strange happenings in their small town.
In late 2010, Fanning began working on Francis Ford Coppola’s new film Twixt, that Coppola wrote, based on a dream he had. She plays the role of a young ghost named V.
In December 2011, Fanning appeared in Cameron Crowe’s We Bought a Zoo. She played Lily, a thirteen-year-old who is working illegally at the zoo’s restaurant, and lives on the property with her only parental figure, Kelly (Scarlett Johansson).
In September 2012, Fanning starred as Ginger along with Alice Englert who played Rosa in the drama film Ginger & Rosa that took place during 1962 in London. The film was directed by Sally Potter and was released on October 19, 2012. Fanning has received widespread acclaim for her performance, with A. O. Scott of The New York Times writing that she “shows a nearly Streepian mixture of poise, intensity and technical precision. It is frightening how good she is and hard to imagine anything she could not do.” Ty Burr, film critic for The Boston Globe, praised her “luminous naturalism that seems the opposite of performance” and felt that “Fanning easily convinces you of Ginger’s emotional reality.”
Fanning also starred alongside Angelina Jolie in the 2014 Walt Disney film, Maleficent, directed by Robert Stromberg. Jolie played Maleficent, while Fanning played Princess Aurora, the Sleeping Beauty. She will co-star in Ben Affleck’s Live by Night, scheduled for release in October 2017.
In April 2016, Fanning was cast in Shawn Christensen’s feature length drama, Sidney Hall.