She appeared in several other films as a child actress, including Daddy Day Care (2003), Babel (2006), The Curious Case of Benjamin Button and Phoebe in Wonderland (both 2008), and the miniseries The Lost Room (2006).

[vague][13] She began her acting career by starring as the younger versions of her older sister Dakota's characters in the miniseries Taken and the film I Am Sam.

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.

In early 2005, Fanning filmed scenes in Charlotte's Web as the "future granddaughter" of Fern Arable played by Dakota.

The plot centers around a "bad-boy"[clarification needed] actor who is forced to re-evaluate his life when his daughter, played by Fanning, arrives unexpectedly.

[25] 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.

"[26] 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.

"[27] Fanning starred alongside Angelina Jolie in the 2014 Walt Disney film Maleficent, directed by Robert Stromberg.

[39] In 2017, Fanning appeared in Shawn Christensen's feature-length drama The Vanishing of Sidney Hall,[40] which premiered on January 25 at the Sundance Film Festival.

[41] In the same year, Fanning appeared in John Cameron Mitchell's British-American science-fiction romantic comedy film How to Talk to Girls at Parties (based on a short story by Neil Gaiman), reuniting with Sofia Coppola in The Beguiled, in the Irish-American romance film Mary Shelley, directed by Haifaa al-Mansour, and in the music video for Grouplove's single "Good Morning".

[44] She also starred in Galveston opposite Ben Foster, directed by Mélanie Laurent, which had its world premiere at South by Southwest on March 10, 2018.

[45] That same year, Fanning starred in Teen Spirit, directed by Max Minghella, which had its world premiere at the Toronto International Film Festival in September 2018.

[48] That same year, Fanning starred in Woody Allen's romantic comedy film A Rainy Day in New York alongside Timothée Chalamet and Selena Gomez.

[54][55] She received critical acclaim for the role and was nominated in the 2021 Golden Globe Award for Best Actress – Television Series Musical or Comedy.

[3] Her performance also earned Fanning her first Primetime Emmy Award nomination for Outstanding Lead Actress in a Comedy Series.

[59][60] Fanning and her sister Dakota started Lewellen Pictures with a first look deal at MRC, and served as executive producers on Mastermind: To Think Like a Killer (2024) for Hulu.

[61][62][63] Fanning is set to take a starring role in video game director Hideo Kojima's next project, Death Stranding 2: On the Beach.

In September Fanning began filming Rosebush Pruning[68] by Karim Ainouz, a remake of Fists in the Pocket by Marco Bellocchio.