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Dennings played Norah Silverberg, the daughter of a famous record producer, and was nominated for the International Press Academy's Satellite Award for Best Actress for the performance.
In September 2008, Dennings hoped to make Don De Lillo's novel End Zone into a film.
In 2002, Dennings appeared in the Disney Channel film The Scream Team as a teenager who stumbles into a group of ghosts.
She was cast for a five-episode run on The WB's Everwood, but the role was recast with Nora Zehetner.
After making her acting debut in an episode of the HBO dramedy series Sex and the City, Dennings has since appeared in films including The 40-Year-Old Virgin (2005), Big Momma's House 2 (2006), Charlie Bartlett (2007), The House Bunny (2008), Nick and Norah's Infinite Playlist (2008), Defendor (2009), Thor (2011) and Thor: The Dark World (2013).
In 2009, Dennings appeared in The Answer Man, a story about a celebrity author whose manifestos become a sort of new Bible.
The film began production in Orlando, Florida, in February 2011.
Dennings stated to The Jewish Journal of Greater Los Angeles that Judaism "is an important part of my history, but, as a whole, religion is not a part of my life." The article went on to say that she considers herself more ethnically and culturally affiliated than religiously so.
Dennings continued working on television, guest-starring on Without a Trace as a teen whose boyfriend goes missing, and on Less than Perfect in 2003.
In February 2004, she was cast in a pilot for CBS titled Sudbury, about a family of modern-day witches, based on the 1998 film Practical Magic, but the series was not picked up.