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After graduating from Barnard College in 1993, Babbit's first job was as an assistant to the assistant for Martin Scorsese on The Age of Innocence. After that she worked as an intern on John Sayles's The Secret of Roan Inish where she worked with fellow aspiring filmmakers Karyn Kusama and Jasmine Kosovic.
Babbit's next job was as script supervisor on John Duigan's film The Journey of August King-a job for which she had little experience, that she said she "lied her way into". This was followed by Su Friedrich's television film Hide and Seek. In 1996, after working on If These Walls Could Talk, where she met her future partner Andrea Sperling, Babbit got a job as script supervisor on David Fincher's film The Game. This proved to be influential to her career as a director.
In 1996, Babbit, with Ari Gold, directed Frog Crossing, a comedic short film about an animal rights activist who protects frogs as they hop across a highway. She followed this with 1999 comedy short Sleeping Beauties. While working on The Game, she discussed her idea for a short film based on a fairy tale with Fincher. He gave Babbit about 6,000 feet of 35 mm film. His editor gave her free use of an Avid editing machine. The star of The Game, Michael Douglas, wrote to Paramount and asked them to let Babbit access their costume department. As a result, she was able to make Sleeping Beauties for about $10,000. Based on the classic fairy tale Sleeping Beauty, the film is about a young woman (Sarah Lassez) who works as a makeup artist at a funeral home. Obsessed with an unavailable ex-girlfriend, she eventually meets and falls in love with a photographer's assistant (Clea DuVall). The short premiered at Sundance in 1995. Her other short film Stuck premiered at Sundance in 2002 and won a jury prize.
In 1999, Babbit directed her first feature film, But I'm a Cheerleader. Starring Natasha Lyonne and Clea DuVall, it is a romantic comedy about a high school cheerleader who is sent to a so-called "reparative therapy" camp when her parents suspect she is a lesbian. The film was inspired by an article that Babbit read about a man who had been sent to a similar camp. The camp in the film was partly based on a halfway house for young people with drug and alcohol problems run by her mother. Babbit appeared in This Film Is Not Yet Rated discussing this film and her struggle against an NC-17 rating. In 2000, the film won the Audience Award and the Graine de Cinéphage Award at the Créteil International Women's Film Festival, an annual French festival which showcases the work of female directors. Film scholar Wheeler Winston Dixon described the film as a commercial and critical success which became a cult film on DVD in later years.
Babbit's second film was 2005 thriller film The Quiet. Starring Elisha Cuthbert and Camilla Belle, the plot revolves around a deaf girl who, when sent to live with her godparents, discovers some dark secrets about the family. The film's worldwide rights was acquired by Destination Films, which released this film in the United States theatrically through Sony Pictures Classics. The film was not generally well received by critics, but still became a commercial success.
Babbit's next film, comedy Itty Bitty Titty Committee was released in 2007. Produced by POWER UP, it starred Melonie Diaz as a young woman who becomes involved with a radical feminist group. It received mostly negative reviews but was nominated for a Teddy Award at the Berlin International Film Festival and won a jury award at South by Southwest in 2007.
In 2011 Babbit began production on Breaking the Girls, a thriller film written by Mark Distefano and Guinevere Turner. It was released in 2012.
Babbit has directed and produced episodes of several television programs including Popular, United States of Tara, The Bernie Mac Show, Malcolm in the Middle, Nip/Tuck, Gilmore Girls, Castle, Alias, Ugly Betty, Dirty Sexy Money, Drop Dead Diva, Looking, Girls, The Marvelous Mrs. Maisel, and The L Word. She enjoys working in television because it helps her to "keep her skills up". She has said that because television directors have less overall responsibility than film directors, she is able to concentrate on working with actors. Television work also enables her to earn money while pursuing her long-term goals of making feature films.