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Foster began her professional career as a child model and later as a teen idol in various Disney films including Napoleon and Samantha (1972), Freaky Friday (1976) and Candleshoe (1977). She acted in Martin Scorsese's comedy-drama Alice Doesn't Live Here Anymore (1974) and reunited with him in Taxi Driver (1976) in a role for which she received an Academy Award for Best Supporting Actress nomination. Other early films include Tom Sawyer (1973), Bugsy Malone (1976), The Little Girl Who Lives Down the Lane (1976), Carny (1980) and Foxes (1980).

After attending Yale University, Foster transitioned into mature leading roles earning two Academy Awards for playing a rape victim in The Accused (1988), and Clarice Starling in The Silence of the Lambs (1991). She also received a nomination for Nell (1994). Her other notable films include Sommersby (1993), Maverick (1994), Contact (1997), Anna and the King (1999), Panic Room (2002), Flightplan (2005), Inside Man (2006), The Brave One (2007), Nim's Island (2008), Carnage (2011), Elysium (2013), Hotel Artemis (2018), and The Mauritanian (2021).

She made her directorial film debut with Little Man Tate (1991) and has since directed films such as Home for the Holidays (1995), The Beaver (2011) and Money Monster (2016). She founded her own production company, Egg Pictures, in 1992. She earned two Primetime Emmy Awards for producing The Baby Dance (1999), and directing the Orange Is the New Black episode "Lesbian Request Denied" in 2014. She has also directed episodes for Tales from the Darkside, House of Cards, Black Mirror, and Tales from the Loop.

Foster's sexual orientation became the subject of public discussion in 1991 when publications such as OutWeek and The Village Voice, protesting against the alleged homophobia and transphobia in The Silence of the Lambs, claimed she was a lesbian. She publicly acknowledged her 14-year relationship with Cydney Bernard in 2007 in a speech at The Hollywood Reporter's "Women in Entertainment" breakfast honoring her. In 2013, she addressed her decision to come out in a speech after receiving the Cecil B. DeMille Award at the 70th Golden Globe Awards, which led many news outlets to describe her as gay. Some sources noted that she did not use the words "gay" or "lesbian" in her speech.