Fanning started acting before turning three years old. She began her acting career by playing the younger version of her older sister Dakota's characters in the mini-series Taken and the movie I Am Sam. In 2002, at the age of four, Fanning won her first role independent of her sister in the comedy Daddy Day Care. 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 opposite Jeff Bridges and Kim Basinger. The film's producers 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 voice work in the English dubbed version of Miyazaki's animated film My Neighbor Totoro, in the role of Mei, opposite Dakota who voiced Satsuki, the older sister to Elle's character. 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. However, the scenes did not 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 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: MD, playing the patient's daughter. She also appeared in an of Criminal Minds in 2006, playing the supporting role of Tracey in "The Boogeyman".

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 which Emma's brother is killed. In early 2007, Fanning reunited with her Babel co-stars, Brad Pitt and Cate Blanchett, in a small part in The Curious Case of Benjamin Button as the younger version of Blanchett's character. Mid-year 2007, Fanning filmed the title role Phoebe of Phoebe in Wonderland. 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. 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 2010 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. In late 2010, Fanning began working on Francis Ford Coppola's 2011 film Twixt, which Coppola based on a dream. She plays the role of a young ghost named "V". In 2011, Fanning starred in J. J. Abrams' sci-fi-drama film Super 8 as Alice Dainard. The film 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 December 2011, Fanning appeared in Cameron Crowe's We Bought a Zoo. She played Lily, a thirteen-year-old who is working 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 at the 2014 San Diego Comic-Con promoting The Boxtrolls. 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.

In 2015, Fanning co-starred in Jay Roach's Trumbo as Dalton Trumbo's (Bryan Cranston) daughter Nikola.

In 2016, she appeared as Jesse in the psychological thriller The Neon Demon, directed by Nicholas Winding Refn. The film had its world premiere at the Cannes Film Festival in May 2016. It was released on June 24, 2016, and did poorly at the box office. That same year, she appeared in Mike Mills's 20th Century Women, opposite Greta Gerwig and Annette Benning. The film had its world premiere at the New York Film Festival on October 8, 2016, and began a limited release on December 28, 2016. She then co-starred in Ben Affleck's Prohibition-era drama Live by Night, which was released on December 25, 2016.

In 2017, Fanning appeared in Shawn Christensen's feature-length drama, Sidney Hall, which premiered on January 25 at the Sundance Film Festival.

Fanning currently has three films in post-production, including I Think We're Alone Now, Galveston and Mary Shelley.

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