Along with his collaborator D. B. Weiss, he is best known for co-creating Game of Thrones (2011–2019), the HBO adaptation of George R. R. Martin's series of books A Song of Ice and Fire.

Benioff was born David Friedman in New York City, the youngest of three children in a Jewish family with ancestral roots in Austria, Romania, Germany, Poland and Russia.

[6] He has two older sisters, Suzy and Caroline,[7] and grew up in Manhattan, first in Peter Cooper Village, then on 86th Street where he spent most of his childhood, before eventually moving near the U.N. headquarters when he was 16.

[8][9] Benioff became interested in an academic career and went to Trinity College, Dublin (TCD), in 1995, for a one-year program to study Irish literature.

[8] He worked as a radio DJ in Moose, Wyoming, for a year—mostly as a side job that he accepted mainly to spend a year in the countryside at a writer's retreat.

[1] Benioff spent two years writing his first published novel, The 25th Hour,[16][17] originally titled Fireman Down, and completed the book as his thesis for his master's degree at Irvine.

[27] Benioff had aimed for a "darker and a bit more brutal" story, writing it with an R rating in mind, but acknowledged the film's final tone would rest with the producers and director.

[31][32] In April 2014, Benioff announced he and Weiss had taken on their first feature film project to write, produce, and direct Dirty White Boys, based on a novel by Stephen Hunter.

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.

[37] In February 2018, Disney announced that Benioff and Weiss would write and produce a new series of Star Wars films after the final season of Game of Thrones ended in 2019.

[41] In early August 2019, Benioff and Weiss negotiated an exclusive multi-year film and television deal with Netflix worth $200 million.

[47] In September 2020, it was announced that Benioff, Weiss and Alexander Woo will write and executive produce a Netflix series based on The Three-Body Problem trilogy.