Mamet was born in 1947 in Chicago to Jewish parents, Lenore June (née Silver), a Teacher, and Bernard Morris Mamet, a labor attorney. One of his first jobs was as a busboy at Chicago's London House and The Second City. He also worked as an actor, Editor for Oui magazine and cab-driver. He was educated at the progressive Francis W. Parker School and at Goddard College in Plainfield, Vermont. At the Chicago Public Library Foundation 20th anniversary fundraiser in 2006, though, Mamet announced "My alma mater is the Chicago Public Library. I got what little educational foundation I got in the third-floor reading room, under the tutelage of a Coca-Cola sign".

Mamet and Actress Lindsay Crouse were married in 1977 and divorced in 1990. He and Crouse have two children, Willa and Zosia. Willa is a professional Photographer and Zosia is an Actress. Mamet has been married to Actress and singer-songwriter Rebecca Pidgeon since 1991. They have two children, Clara and Noah.

Mamet's first produced screenplay was the 1981 production of The Postman Always Rings Twice (directed by Bob Rafelson), based upon James M. Cain's novel. He received an Academy Award nomination one year later for his first script, The Verdict, written in the late 1970s. He also wrote the screenplay for The Untouchables.

Mamet dedicated Glengarry Glen Ross to Harold Pinter, who was instrumental in its being first staged at the Royal National Theatre, (London) in 1983, and whom Mamet has acknowledged as an influence on its success, and on his other work.

Mamet wrote the "Wasted Weekend" episode of Hill Street Blues that aired in 1987. His then-wife, Lindsay Crouse, appeared in numerous episodes (including that one) as Officer McBride. Mamet is also the creator, Producer and frequent Writer of the television series The Unit, where he wrote a well-circulated memo to the writing staff. He directed a third-season episode of The Shield with Shawn Ryan. In 2007, Mamet directed two television commercials for Ford Motor Company. The two 30-second ads featured the Ford Edge and were filmed in Mamet's signature style of fast-paced dialogue and clear, simple imagery. Mamet's sister, Lynn, is a Producer and Writer for television shows, such as The Unit and Law & Order.

Mamet's plays have frequently sparked debate and controversy. During a staging of Oleanna in 1992, in which a post-secondary student accuses her professor of sexual harassment, a critic reported that the play divided the audience by gender and recounted "couples emerged screaming at each other".

Mamet's books include: The Old Religion (1997), a novel about the lynching of Leo Frank; Five Cities of Refuge: Weekly Reflections on Genesis, Exodus, Leviticus, Numbers and Deuteronomy (2004), a Torah commentary with Rabbi Lawrence Kushner; The Wicked Son (2006), a study of Jewish self-hatred and antisemitism; Bambi vs. Godzilla, a commentary on the movie business; The Secret Knowledge: On the Dismantling of American Culture (2011), a commentary on cultural and political issues; and Three War Stories (2013), a trio of novellas about the physical and psychological effects of war.

Mamet remains a Writer and Director, and has assembled an informal repertory company for his films, including Crouse, william H. Macy, Joe Mantegna, Rebecca Pidgeon, and Ricky Jay, as well as some of the aforementioned poker associates. Mamet has funded his own films with payments he receives for credited and uncredited rewrites of typically big-budget films. For instance, Mamet did a rewrite of the script for Ronin under the pseudonym “Richard Weisz” and turned in an early version of a script for Malcolm X that Director Spike Lee rejected. In 2000, Mamet directed a film version of Catastrophe, a one-act play by Samuel Beckett featuring Harold Pinter and John Gielgud (in his final screen performance). In 2008, he directed and wrote the mixed martial arts movie Redbelt, about a martial arts instructor tricked into fighting in a professional bout. Mamet teamed up with his wife Rebecca Pidgeon to adapt the novel Come Back to Sorrento as a screenplay. The film was in development during 2010. He is also Director of the TV film Phil Spector.

In 2002, Mamet was inducted into the American Theatre Hall of Fame. Mamet later received the PEN/Laura Pels International Foundation for Theater Award for Grand Master of American Theater in 2010.

Since May 2005 he has been a contributing Blogger at The Huffington Post, drawing satirical cartoons with themes including political strife in Israel. In a 2008 essay at The Village Voice titled Why I Am No Longer a 'Brain-Dead Liberal' he revealed that he had gradually rejected political correctness and progressivism and embraced conservatism. Mamet has spoken in interviews of changes in his views, highlighting his agreement with free market theorists such as Friedrich Hayek the Historian Paul Johnson, and Economist Thomas Sowell, whom Mamet called "one of our greatest minds".

The papers of David Mamet were sold to the Harry Ransom Center at the University of Texas at Austin in 2007 and first opened for research in 2009. The growing collection consists mainly of manuscripts and related production materials for most of his plays, films, and other writings, but also includes his personal journals from 1966 to 2005. In 2015, the Ransom Center secured a second major addition to Mamet's papers that include more recent works. Additional materials relating to Mamet and his career can be found in the Ransom Center's collections of Robert De Niro, Mel Gussow, Tom Stoppard, Sam Shepard, Paul Schrader, Don DeLillo, and John Russell Brown.

Mamet is a founding member of the Atlantic Theater Company; he first gained acclaim for a trio of off-Broadway plays in 1976, The Duck Variations, Sexual Perversity in Chicago, and American Buffalo. He was awarded the Pulitzer Prize in 1984 for Glengarry Glen Ross, which received its first Broadway revival in the summer of 2005. His play Race, which opened on Broadway on December 6, 2009 and featured James Spader, David Alan Grier, Kerry Washington, and Richard Thomas in the cast, received mixed reviews. His play The Anarchist, starring Patti LuPone and Debra Winger, in her Broadway debut, opened on Broadway on November 13, 2012 in previews and was scheduled to close on December 16, 2012. His 2017 play The Penitent previewed off-Broadway on February 8, 2017.

In 1990 Mamet published The Hero Pony, a 55-page collection of poetry. He has also published a series of short plays, monologues and four novels, The Village (1994), The Old Religion (1997), Wilson: A Consideration of the Sources (2000), and Chicago (2018). He has written several non-fiction texts, and children's stories, including "True and False: Heresy and Common Sense for the Actor"(1997). In 2004 he published a lauded version of the classical Faust story, Faustus, however, when the play was staged in San Francisco during the spring of 2004, it was not well received by critics. On May 1, 2010, Mamet released a graphic novel The Trials of Roderick Spode (The Human Ant).

On June 2, 2011, The Secret Knowledge: On the Dismantling of American Culture, Mamet's book detailing his conversion from modern liberalism to "a reformed liberal" was released.

In November 2012 Mamet penned an article for The Jewish Journal of Greater Los Angeles imploring fellow Jewish Americans to vote for Republican nominee Mitt Romney.

In an essay for Newsweek, published on 29 January 2013, Mamet argued against gun control laws: "It was intended to guard us against this inevitable decay of government that the Constitution was written. Its purpose was and is not to enthrone a Government superior to an imperfect and confused electorate, but to protect us from such a government."

Arthur Holmberg in his 2014 book David Mamet and Male Friendship, has reconsidered the gender issue in many of Mamet's plays throughout his career by asserting a prominent and recurrent reversed sexual orientation of portrayed male gender preferences.

In 2017, Mamet released an online class for Writers entitled David Mamet teaches dramatic writing.