He is also best known for providing the English voices of Solid Snake and Naked Snake in the Metal Gear video game series.He also wrote the screenplay for Watchmen from the comic book series of the same name, which received an enthusiastic reception from the director and original illustrator. Earlier in his acting career, he played the lead role in the live-action Guyver: Dark Hero.

Hayter was born in 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 in 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, 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 making a cameo appearance 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, taking over the role of protagonist Sean Barker from previous actor Jack Armstrong.

In 1998, Hayter voiced protagonist Solid Snake in the highly successful video game Metal Gear Solid. He provided Snake's voice in later Metal Gear games such as Metal Gear Solid 2: Sons of Liberty and Metal Gear Solid: The Twin Snakes (which was a remake of Metal Gear Solid), and provided the voice for a closely related character, Naked Snake, a young Big Boss, in the prequels Metal Gear Solid 3: Snake Eater and Metal Gear Solid: Portable Ops. Afterward, he voiced Solid Snake (renamed Old Snake) in Metal Gear Solid 4: Guns of the Patriots and Naked Snake (renamed simply Snake) in Metal Gear Solid: Peace Walker. Hayter also had an extended cameo as himself in Metal Gear Solid 4: Guns of the Patriots during one of the live-action sequences 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. Hayter also provided the voice of Solid Snake for the character's guest appearance in Super Smash Bros. Brawl, a Wii fighting game featuring various Nintendo characters.

Hayter is one of the few Metal Gear Solid actors to date that have played and beaten the Metal Gear games he's voiced in, while co-star Christopher Randolph has only played Metal Gear Solid.

According to an interview with Paul Eiding, Hayter gave up half of his own paycheck in order to bring back the cast of Metal Gear Solid for the Nintendo GameCube version, The Twin Snakes. This is the reason why the voice acting in The Twin Snakes was almost completely redone with the same voice actors, one of the few differences being the actor for Gray Fox, Greg Eagles, who was replaced by Rob Paulsen.

His work with Metal Gear Solid has also led Hayter to do voice work in other video game projects such as Eternal Darkness: Sanity's Requiem and Star Wars: The Old Republic. He also cited the Metal Gear Solid series as an influence on his screenwriting, stating that "Kojima and I have different styles," "but I've certainly learned things from him, especially about ambiguity and telling a story without giving all the answers."

After the announcement of Metal Gear Solid V: The Phantom Pain, Hayter said he was not asked to reprise his role as Big Boss/Snake.This was later confirmed on June 6, when Konami announced that Kiefer Sutherland would be the new voice of Snake

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.

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 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.

On April 12, 2011, it was announced that Hayter has been tapped to write the feature film screenplay for the science fiction/fantasy novel Dragonflight by Anne McCaffrey.

On September 7, 2012, it was announced that Hayter would pen the screen adaptation Caught Stealing, and would star Patrick Wilson and Alec Baldwin.

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

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