Benioff was born David Friedman in New York City, to a Jewish family with roots in Romania, Austria, Poland and Russia. He is the son of Barbara (Benioff) and Stephen Friedman, who is a former head of Goldman Sachs. As an adult, he uses the last name of Benioff, his mother's maiden name, to avoid confusion with other writers named David Friedman.￼
Benioff spent two years writing his first published novel The 25th Hour, originally titled Fireman Down, and completed the book as his thesis for his master's degree at Irvine. He was asked to adapt the book into a screenplay after Tobey Maguire read a preliminary trade copy and became interested in making a film of the book. It was filmed as 25th Hour, starring Edward Norton and directed by Spike Lee. He then wrote a collection of short stories titled When the Nines Roll Over (And Other Stories) in 2004.
Benioff drafted a screenplay of the mythological epic Troy (2004) for which Warner Bros pictures paid him $2.5 million. He also wrote the script for the psychological thriller Stay (2005), which was directed by Marc Forster and starred Ewan McGregor and Naomi Watts. His screenplay for The Kite Runner (2007), adapted from the novel of the same name, marked his second collaboration with director Marc Forster. He was hired in 2004 to write the screenplay for the X-Men spin-off X-Men Origins: Wolverine (2009), and worked on the script for three years.
In 2006, Benioff became interested in adapting the A Song of Ice and Fire novel series by George R.R. Martin and began working with D. B. Weiss on a proposed television series Game of Thrones. The pilot was put into development by HBO in 2007 and the series greenlit in 2010. They act as the executive producer, showrunner and writer of the show, which began airing on HBO in 2011. Benioff and Weiss had previously worked together on a script for a horror film titled The Headmaster, but it was never made.
In 2008, his second novel, City of Thieves was published. He has been hired by Universal Pictures in October 2007 to write an adapted screenplay of the Charles R. Cross biography of Kurt Cobain but the screenplay was not used.
On April 10, 2014, Benioff announced he and D. B. Weiss had taken on their first feature film project to write, produce and direct Dirty White Boys, a novel by Pulitzer prize-winning author Stephen Hunter. On July 19, 2017, Benioff announced that he and Weiss are going to begin production on another HBO series, titled Confederate, after the final season of Game of Thrones. Benioff and Weiss said, "We have discussed Confederate for years, originally as a concept for a feature film - But our experience on Thrones has convinced us that no one provides a bigger, better storytelling canvas than HBO."
- On September 30, 2006, Benioff married actress Amanda Peet in New York City. Together they have three children: Frances, Molly and Henry. The family lives in Manhattan and Beverly Hills, California.