Howard was born in Los Angeles, California, to writer Cheryl Howard Crew (née Alley) and actor-director Ron Howard, on March 2, 1981. She has two younger sisters, twins Jocelyn and Paige (born 1985), and a younger brother named Reed (born 1987). Through her father, she is a granddaughter of actors Rance Howard and Jean Speegle Howard and a niece of actor Clint Howard. Her godfather is actor Henry Winkler, who co-starred on Happy Days with her father.
All of the Howard children were raised away from the world of show business. Their parents did not allow them access to television and instead encouraged outdoor activities and hobbies. At the age of 7, however, she was allowed to be an extra in her father's movies. In an appearance on The Tonight Show with Jay Leno, she mentioned that she and her siblings were babysat by family friend Tom Cruise on several occasions. She was raised in Westchester County, New York and on a farm in Greenwich, Connecticut.
Howard attended Stagedoor Manor, a performing arts camp in upstate New York, with actress Natalie Portman. After attending Greenwich Country Day School until 1996 and then graduating from Byram Hills High School in 1999, Howard studied at New York University's (NYU) Tisch School of the Arts for three years, during which time she also attended the Stella Adler Conservatory, The Experimental Wing, and International Theatre Wing in Amsterdam. During her schooling, she took part in the concept recording of the Broadway-bound musical A Tale of Two Cities. She graduated with her BFA in Drama in 2003. Howard is also an alumna of the Steppenwolf Theatre Company's School at Steppenwolf in Chicago, and of The Actors Center in New York City. During her time in New York, Howard was also a member of downtown theater company Theater Mitu, in residence at New York Theatre Workshop, who are known for their exploration of theatrical forms.
For several years, Howard appeared in New York plays. Among these were House & Garden, a 2002 Alan Ayckbourn production held at the Manhattan Theatre Club, in which she portrayed a disdainful, flirtatious teen. While performing as Rosalind in the critically acclaimed 2003 William Shakespeare comedy production As You Like It at The Public Theater, Howard caught the eye of director M. Night Shyamalan.
Howard was cast in Shyamalan's fantasy thriller The Village (2004) two weeks later without having to audition. Its story is about a "turn-of-the-20th-century" village whose residents live in fear of the creatures inhabiting the woods beyond it. She plays the female lead, the chief's blind daughter and love interest to Joaquin Phoenix's part. Her performance was applauded by critics and Howard was nominated for several awards, mostly in the category of "Best Breakthrough Performance". The Village did well commercially, but had a mixed reception. Following that, Howard was cast by Lars Von Trier to replace Nicole Kidman as Grace Mulligan in Manderlay, the 2005 sequel to Dogville (2003). The director said that it is "quite clear" his movie, set in a plantation, can be seen as an allusion to the Iraq War.
Howard reunited with Shyamalan for Lady in the Water, in which she acts as Story, a type of water nymph called a narf. The 2006 fantasy film release also stars Paul Giamatti as the co-lead. Shyamalan's project follows the story of Giamatti's character rescuing what he thinks is a young woman (Howard) from his pool. Once he discovers that she is actually a character from a bedtime story who is trying to get back home, he teams up with his tenants to protect her from creatures that try to keep her in their world. It underperformed at the box office, falling short of its $75 million budget, and got largely negative reviews from critics. Next, she once again played Rosalind in Kenneth Branagh's 2006 film version of Shakespeare's As You Like It. It played in theatres in Europe before going directly to cable in the United States, premiering on HBO. Howard was nominated for a Golden Globe Award at the 2008 ceremony. The project got soundly negative reviews from the British media, while American reviewers gave it more favorable notice. That year, she wrote and directed a short film, Orchids, as part of Glamour magazine's "Reel Moments" series funded by Cartier and FilmAid International.
In 2007, Howard starred in her first blockbuster, Spider-Man 3 as Peter Parker's classmate Gwen Stacy, a fan favorite. A challenge that came with playing Gwen was reminding fans of the good-intentioned character who was Peter's first love in the comics, yet came off as "the other woman" in the movie. Howard dyed her naturally red hair blonde for the role and performed many of her own stunts, unaware that she was several months pregnant. Grossing $890 million.Terminator Salvation was her next project. Cast in June 2008, she replaced Claire Danes as Kate Connor. Howard was already a fan of the series. It grossed a total of $370 million, but was not well received critically.
Howard starred as the lead character in The Loss of a Teardrop Diamond in 2009. Based on a 1957 screenplay by Tennessee Williams, it did not play at many theaters. She played the role of Victoria, a vampire seeking revenge, in the Twilight series' third installment The Twilight Saga: Eclipse. She landed the part after Rachelle Lefevre was dropped due to a scheduling conflict and filming started in August 2009. Howard had already been a huge fan of the books and considered Victoria to be an "incredible character". Released on June 30, 2010 the film made nearly $700 million and although reviews were mixed, Critics gave very positive reviews for Howard in the role.
In December 2009, Howard was cast in Clint Eastwood's Hereafter (2010), as a burgeoning love interest for Matt Damon's character.
In early January 2011, Howard became the first celebrity ambassador for purse designer Kate Spade. Her first film of 2011 was The Help, a movie adaptation of Kathryn Stockett's 2009 best-selling novel of the same name. She received critical acclaim for her performance in the film, and was nominated for many Best Supporting Actress Awards, along with winning awards shared with the rest of the cast. Howard then produced Gus Van Sant's Restless, a dark coming of age movie about a teenage boy and girl who are engrossed with death. She had a supporting role opposite Joseph Gordon-Levitt in the cancer dramedy 50/50, which was based on a true story. "It's viewing that experience through a very truthful lens of humour", she stated of 50/50's take on its heavy subject matter. Both films had September releases.
Howard directed the short film When You Find Me, a social film developed through a collaboration with Canon. The film was developed under the premise of gathering inspiration through images selected from a photography contest. 96,362 entries were accepted, while only eight final images were selected to be utilized for the production of the film.
In 2015, Howard appeared in the lead role, alongside Chris Pratt, in Jurassic World as the park's operations manager Claire Dearing. In 2016, she starred in the remake of the 1977 film Pete's Dragon, and appeared in the drama Gold with Matthew McConaughey. In 2016, she appeared in "Nosedive", an episode of the anthology series Black Mirror. In 2017, she started production of the follow up to Jurassic World, currently titled Jurassic World: Fallen Kingdom.
During her senior year of high school, Howard learned of existentialism. "I was like, 'This is it! This is my religion.' I had never felt a connection to any sort of spirituality before that. It was very basic – you're responsible for the choices that you make – but it was mind-blowing at the time."
Howard met actor Seth Gabel at New York University and the two dated for five years before marrying on June 17, 2006. She had only one previous boyfriend and claims to have pursued Gabel vigorously after first meeting him. They had planned to start a family together in their 30s; however, seven days after their wedding, she learned that she was expecting their first child. Howard gave birth to their child, a son named Theodore, nicknamed Theo, in 2007. Howard openly discussed having experienced post-partum depression. With the help of a physician and a therapist she recovered from the depression, which lasted for about 18 months. Howard said of the depression in 2010,
Do I wish I had never endured post-partum depression? Absolutely. But to deny the experience is to deny who I am. I still mourn the loss of what could have been, but I also feel deep gratitude for those who stood by me, for the lesson that we must never be afraid to ask for help, and for the feeling of summer that still remains.
Howard gave birth to the couple's second child, daughter Beatrice, in 2012.