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In New York City, Garner earned $300 a week as an understudy in the play A Month in the Country for Roundabout Theatre Company in 1995. She was then cast in her first television role, a part in the made-for-television movie Zoya, based on the Danielle Steel novel. In 1996 she appeared in an episode of Spin City as the character James' high school sweetheart and in an episode of Law & Order as a temporary love interest of Benjamin Bratt's character. Her next acting jobs were in two short-lived television series, Significant Others and Time of Your Life, and a recurring role in the series Felicity. Garner appeared in the comedy Dude, Where's My Car?, playing Ashton Kutcher's girlfriend. In 2001, she appeared as a nurse in the big-budget epic Pearl Harbor, co-starring with Kate Beckinsale and future husband Ben Affleck.
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Catch and Release, a romantic comedy, opened on January 26, 2007. Garner has formed a production company named Vandalia Films which will produce its first film in 2007. She will produce the company's upcoming films Sabbatical and Be with You. Garner took her first role as part of an ensemble in The Kingdom alongside Jamie Foxx, Jason Bateman and Ashraf Barhom. Box office analysts have commented that the choice was a smart move on Garner's part, as her other projects with her as the sole lead are risky gambles. Garner was set to star in Zach Braff's directorial feature of Open Hearts but backed out of the project so she could spend more time with her family.
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In 2008, Garner appeared as a presenter at the Oscars. However, for Garner, this part of the evening was somewhat overshadowed in the next day's press by discussions of the unexpected interruption of her Red Carpet interview by Gary Busey. Busey later publicly apologized for the incident, saying that he merely wanted to congratulate Laura Linney, who was being interviewed along with Garner, and didn't realise that they were being interviewed at the time. In 2009, she appeared in the films Ghosts of Girlfriends Past and The Invention of Lying.
Garner played Roxanne in Cyrano de Bergerac at the Richard Rodgers Theatre on Broadway from November 1, 2007 alongside Kevin Kline who was in the title role. This was her Broadway debut. The show was originally set to run until December 23, 2007, but it was extended through January 6, 2008 due to the Broadway stagehand strike in late 2007. For this role Garner won the 9th Annual broadway.com Audience Award for Favorite Actress in a Play.