Hayter also wrote an adaptation of the graphic novel Watchmen by Alan Moore and David Gibbons. Noted for being a harsh critic of translations of his works to film, Moore said of the script "David Hayter's screenplay was as close as I could imagine anyone getting to [a film version of] Watchmen. That said, I shan't be going to see it. My book is a comic book. Not a movie, not a novel. A comic book. It's been made in a certain way, and designed to be read a certain way." Hayter and Writer Alex Tse shared credit on the finished screenplay. Tse drew "the best elements" from two of the project's previous drafts written by Screenwriter Hayter. The script did not keep the contemporary atmosphere that Hayter created, but instead returned to the original Cold War setting of the Watchmen comic. Warner Bros. was amenable to the 1980s setting, and the Director also added a title montage sequence to introduce the audience to the events of alternate history United States in that time period.

Hayter was born in Santa Monica, California to Canadian parents. He started acting at the age of 9. Hayter spent most of his childhood living around the world and at the age of 15, Hayter moved to Kobe, Japan where he graduated from the Canadian Academy, an international school, in 1987. After high school, he attended Rensselaer Polytechnic Institute for two years until transferring to Ryerson University in Toronto, Ontario, Canada where he stayed until the age of 20, when he moved to Hollywood.

Hayter did some live acting in the early 1990s, but became interested in voice acting after acting in an episode of the sitcom Major Dad, and later landed the role of Captain America in the popular 1994 Spider-Man animated series. He also provided the voice of Arsène Lupin III in the English version of the anime film The Castle of Cagliostro and the voice of Tamahome in the English version of the anime series Fushigi Yūgi. He also starred in the 1994 straight-to-video movie Guyver: Dark Hero as the protagonist Sean Barker (a role he took from actor Jack Armstrong), and have used the characters' name as an alias in various work credits.

In 1998, Hayter voiced protagonist Solid Snake in the highly successful video game Metal Gear Solid. He would reprise the role in Metal Gear Solid 2: Sons of Liberty, Metal Gear Solid: The Twin Snakes (a remake of the original), Super Smash Bros. Brawl and Metal Gear Solid 4: Guns of the Patriots (where the character appears in aged form as Old Snake). Hayter also voiced Naked Snake, a young version of Solid Snake's "father" Big Boss, who serves as the protagonist in Metal Gear Solid 3: Snake Eater, Metal Gear Solid: Portable Ops and Metal Gear Solid: Peace Walker, which were prequels set prior to the events of the original Metal Gear. Hayter has an extended live-action cameo as himself in Metal Gear Solid 4 in one of the fictional TV programs prior to the start of the game. In the scene, he wears the "Solid Eye", the technologically advanced eye patch that Old Snake wears throughout the game.

In 2000 he wrote the screenplay for the movie version of X-Men, and then went on to co-write the screenplay for its sequel X2 with writing team Michael Dougherty and Dan Harris. Shortly after his work on X-Men, Hayter was hired to write and direct a project based on the heroine Black Widow. However, due to the limited success of similar themed films featuring female vigilante protagonists at the time, Marvel withdrew their offer to Hayter stating, "We don’t think it’s time to do this movie". Hayter's daughter Natasha, born whilst he was writing the Black Widow script, is named after the titular character.

On September 13, 2012, Hayter began filming on his directorial debut, Wolves.

On August 7, 2013, it was announced Hayter was developing a television show on Fox tentatively titled World War III, about a fiction global conflict that chronicles “a perfect storm of world events places us in the center of a global battle which may bring the world as we know it to an end.” Hayter will be writing the series' story bible and pilot episode, as well as producing and serving as showrunner.