She appeared in several of her father's films as an extra before her feature film début came in director Alan Brown's 2004 drama, Book of Love. She also appeared in numerous productions on the New York stage, but her breakthrough role came in M. Night Shyamalan's The Village, which she was cast in without having to audition after Shyamalan saw her in a Broadway show. Following that, Howard was cast by Lars Von Trier to replace Nicole Kidman as Grace in Manderlay (2005). She collaborated again with Shyamalan in the 2006 release Lady in the Water, in which she plays Story, a type of water nymph called a "narf."
In 2006 she starred as Rosalind in Kenneth Branagh's film version of Shakespeare's As You Like It, opposite David Oyelowo as Orlando. The film played theatres in Europe, but went directly to cable in the U.S. Ms. Howard was nominated for a Golden Globe Award for her performance.
In May 2007 she appeared as Peter Parker's new love interest Gwen Stacy in Sam Raimi's Spider-Man 3 starring Tobey Maguire and Kirsten Dunst. She dyed her naturally red hair blonde for the role (while the naturally blonde Dunst's hair is dyed red for the role of Mary Jane Watson). Howard won the role and beat out Elisha Cuthbert and Sienna Miller for the part.
She will play the lead role in her upcoming film, The Loss of a Teardrop Diamond, co-starring Chris Evans, Ellen Burstyn and David Strathairn. She landed the role after Lindsay Lohan dropped out.
She wrote and directed a short film, Orchids, starring Alfred Molina as part of Glamour magazine's "Reel Moments" series funded by Cartier and FilmAid International.
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