Flockhart played the role of Helena in A Midsummer Night's Dream, a 1999 film version of Shakespeare's play. In 2000, she appeared in Things You Can Tell Just by Looking at Her and Bash: Latter-Day Plays, later accompanying Eve Ensler to Kenya in order to protest violence against women, particularly female genital mutilation. Flockhart also starred in the off-Broadway production of Ensler's The Vagina Monologues.
In 2004, Flockhart appeared as Matthew Broderick's deranged girlfriend in The Last Shot. In the same year, Flockhart traveled to Spain for the filming of Fragile, which premiered in September 2005 at the Venice Film Festival. She was offered the role of Susan Mayer on Desperate Housewives but declined, and the role later went to Teri Hatcher.
In 2014, Flockhart landed a role in Full Circle's second season, as mob boss Ellen. It was expected to air in 2015. This had been Flockhart's first acting role in three years, after her hiatus when Brothers & Sisters ended.
In 2015, Flockhart was cast in the television series Supergirl as Cat Grant, a "self-made media magnate and founder of CatCo" and boss to Kara (Supergirl's alter ego). The series premiered on October 26, 2015, on CBS. Due to the network's wish to reduce the show's budget, it was moved to sister network The CW after its first season, along with a move to filming in Vancouver. Flockhart remained with the show (albeit as a recurring character), despite her previous aversion to working outside Los Angeles.
In 2022, she played the role of Martha opposite Zachary Quinto in Edward Albee's Who's Afraid of Virginia Woolf at the Geffen Playhouse in Los Angeles. The production was directed by Gordon Greenberg and also starred Aimee Carrero and Graham Philips.
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