Singer wrote and directed his first film in 1988 after graduating from university. His next film, Public Access (1993), was a co-winner of the Grand Jury Prize at the 1993 Sundance Film Festival. In the mid-1990s, Singer received critical acclaim for directing the neo-noir crime thriller The Usual Suspects (1995), which starred Gabriel Byrne, Kevin Spacey, Chazz Palminteri, Kevin Pollak, Pete Postlethwaite, Stephen Baldwin, and Benicio del Toro. He followed this with another thriller, Apt Pupil (1998), an adaptation of a Stephen King short story about a boy's fascination with a Nazi war criminal.
Singer was born in New York City, and was adopted by Grace Sinden, an environmental activist, and Norbert Dave Singer, a corporate executive. He grew up in a Jewish household in West Windsor Township, New Jersey. He attended West Windsor-Plainsboro High School South (formerly just West Windsor-Plainsboro High School), graduating in 1984. For college, Singer studied filmmaking for two years at New York's School of Visual Arts and later transferred to the USC School of Cinematic Arts in Los Angeles. Actors Lori and Marc Singer are his cousins.
After graduating from university, Singer directed a short film in 1988 called Lion's Den involving a number of friends, including actor Ethan Hawke whom he knew from his childhood in New Jersey and editor John Ottman who he had met while working on a friend's short film. After a screening of Lion's Den, Singer was approached by someone who knew of a Japanese company that funded low-budget films. Singer wrote the concept for Public Access (1993) with high school friend Christopher McQuarrie, and fellow USC student Michael Feit Dougan wrote the first draft in ten days about a supposedly idyllic small town. Ottman again served as editor but this time also composed the score for the film. At the 1993 Sundance Film Festival, the film was named as co-winner of the Grand Jury Prize.
Singer followed this by directing The Usual Suspects, which was screened out of competition at the 1995 Cannes Film Festival. It was a success, garnering significant praise and winning McQuarrie an Academy Award for Best Writing (Original Screenplay), and actor Kevin Spacey an Academy Award for Best Supporting Actor.
In early 2001, Singer was planning to direct Confessions of a Dangerous Mind with Johnny Depp in the lead role, from Charlie Kaufman's script based on the Chuck Barris book of the same name. Financial troubles delayed production and Singer moved on. The film was later directed by George Clooney for Miramax Films with Sam Rockwell in the lead role. Singer has said that he was "very impressed" by Clooney's debut as a director, and the film itself. In late 2001, Singer was planning to help DeSanto produce a new Battlestar Galactica television series for Studios USA (now NBC Universal Television Studio) and the Fox network. Singer was scheduled to direct the mini-series which would have served as a backdoor pilot for a potential series. Speaking to Variety in February 2001, Singer said he was "confident that the Galactica brand is a sleeping giant. It was a show I watched during its initial run, from the pilot to the final episode. The essence and the brand name is quite potent in a climate where there's a great deficit of sci-fi programming." Despite his enthusiasm, production delays caused by the September 11, 2001 attacks meant Singer had to drop out due to his commitment to direct a sequel of X-Men. Fox then lost interest in Galactica and Studios USA took the project to the Sci Fi Channel and a different production team. This resulted in the new Battlestar Galactica 2003 mini-series and 2004 television series, which ran until 2008. By August 2012 the script was being rewritten, with Singer explaining that "It will exist, I think, quite well between the Glen Larson and Ron Moore universes".
In mid-2004, Singer was in negotiations to direct X-Men: The Last Stand for Fox. Fox and Singer could not come to agreement and, after an extended détente, Singer was offered the chance to direct the new Superman film, which was ready to go. On July 19, 2004, Variety reported that Singer had signed on to direct Superman Returns for Warner Bros. In retaliation, Fox terminated their production deal with Bad Hat Harry Productions, Singer's production company. Superman Returns was filmed in Australia in 2005, and was released on June 28, 2006. Singer claims that though he had not read the comics, he had always admired and identified with the character, citing the fact that he and Superman are both orphans. He instead based Returns on his love of the 1978 film made by Richard Donner.
In August 2009, Universal Pictures announced that Singer would direct and produce a big screen reimagining of the Battlestar Galactica television series of the late-1970s, which would not draw any material from the Syfy Channel reimagined series. On September 10, 2009, it was announced NBC has partnered with Singer and Bryan Fuller to adapt Augusten Burroughs's Sellevision into a series. The one-hour dramatic comedy, to be written by Fuller and directed by Singer, will focus on the inner workings of a fictional home shopping network, according to The Hollywood Reporter. At the premiere of James Cameron's Avatar on December 16, 2009, Singer confirmed that he would be directing Jack the Giant Slayer (2013) for Warner Bros, and that he had signed on to do X-Men: First Class, but conflicts between the two projects led to Singer being only a producer and co-screenwriter on First Class, with Matthew Vaughn taking over directorial duties.
In October 2012, it was announced that Singer would direct the next movie in the series, X-Men: Days of Future Past; Vaughn stayed on as a producer and screenwriter, and the film was released in May 2014. Singer produced the commercials for the ice cream Magnum Gold, which featured Benicio del Toro. In 2012, Singer was the executive producer alongside Jane Lynch of the short film, Ronny and I, directed by Guy Shalem that screened at Outfest and Cannes. Ronny and I was considered a "revolution" in filmmaking due to the fact that the film was shot entirely on a smart phone. Singer directed another X-Men film, X-Men: Apocalypse, that he also produced and co-wrote with Simon Kinberg, Dan Harris, and Michael Dougherty. Days of Future Past stars James McAvoy, Michael Fassbender, Nicholas Hoult, Jennifer Lawrence, and Evan Peters re-teamed with Singer for Apocalypse. In November 2016, it was announced that Singer would direct in the upcoming Queen biopic, Bohemian Rhapsody.
Singer is openly bisexual, and has said that his life experiences of growing up as a minority influenced his movies. In October 2014, it was confirmed he was expecting a child with actress Michelle Clunie. The couple's first son, Dashiell Julius William Clunie-Singer, was born on January 5, 2015.
In 1997, a 14-year-old extra accused Singer of asking him and other minors to film a shower scene in the nude for the film Apt Pupil. A lawsuit was filed but dismissed for insufficient evidence.
In April 2014, Singer was accused in a civil lawsuit of sexual assault of a minor. According to the suit filed by attorney Jeff Herman, Singer is alleged to have drugged and raped actor and model Michael Egan in Hawaii and Los Angeles in the late 1990s. Singer's attorney called the allegations "completely fabricated" and said Singer planned to countersue. Singer denied the allegations in a statement calling them "outrageous, vicious, and completely false." On May 22, 2014, Singer's attorney presented evidence to Federal District Judge Susan Oki Mollway stating that neither Singer nor Egan were in Hawaii at the time. In early August 2014, Egan sought to withdraw his lawsuit via a Request for Court Order of Dismissal, and asked that it be granted "without prejudice or an award of costs or fees, in the interest of justice."
In May 2014, another lawsuit was filed by attorney Jeff Herman on behalf of an anonymous British man. Both Singer and producer Gary Goddard (who was also named separately in the first case) were accused of sexually assaulting "John Doe No. 117." According to the lawsuit, Goddard and Singer met the man for sex when he was a minor and engaged in acts of "gender violence" against him while in London for the premiere of Superman Returns. The charge against Singer in this case was dismissed, at the accuser's request, in July 2014. The case against Goddard remained active.
Singer is cited in the 2014 documentary film on child sexual abuse in Hollywood, An Open Secret, though the film makes no specific allegations against him.