[12] Their names were revealed when they undertook their first tour, which featured Norwegian Christian metal band Extol, and death metal-influenced metalcore band The Agony Scene, and after they hired Jesse Sprinkle on drums, Jon Dunn on bass, and Kris McCaddon, formerly of Embodyment[13] and Society's Finest, on lead guitar.

[12] Demon Hunter returned to the studio to record their second full-length release, Summer of Darkness, with McCaddon contributing, and again with Jesse drumming.

Summer of Darkness hit stores on May 4, 2004, and was a modest success, propelling Demon Hunter into the secular scene, with the addition of the music video "Not Ready to Die" on MTV2's Headbangers Ball[14][15] and Fuse TV, along with single "My Heartstrings Come Undone" being placed on the Resident Evil: Apocalypse soundtrack.

The album featured four guest vocal appearances, including Mike Williams of The Agony Scene on "Beheaded", Brock Lindow of 36 Crazyfists on "Beauty Through The Eyes of a Predator", Howard Jones from Killswitch Engage on "Our Faces Fall Apart", and Trevor McNevan of Thousand Foot Krutch on "Coffin Builder".

In 2005, Demon Hunter went back to The Compound in Seattle, Washington to record their third studio album, entitled The Triptych.

Demon Hunter's only 2006 tour took place over the summer with Zao, Becoming the Archetype, August Burns Red, and Spoken.

The hard rock and heavy metal based magazine, Revolver, published a cover story on Christian metal in December 2006, featuring what the magazine called "The Holy Alliance": Spencer Chamberlain from Underoath, Ryan Clark from Demon Hunter, Tim Lambesis from As I Lay Dying, and Cory Brandan Putman from Norma Jean.

Demon Hunter entered the studio in June 2007 to record their fourth full-length album, Storm the Gates of Hell, which was released on November 6, 2007.

In spite of the bands secular popularity, they continued to support the underground Christian metal scene by appearing on obscure radio programs such as The Full Armor of God Broadcast[18] in January 2008.

Demon Hunter released 45 Days in November 2008, a box set comprising two DVDs and a CD containing a documentary film about the band and their fans, a pro-shot performance from the "Stronger Than Hell" tour, and a brand new score written exclusively for the film along with two bonus tracks.

The album features The Showdown lead guitarist Patrick Judge, who filled in for Luck on several of the "Stronger Than Hell" dates due to Luck's conflicting scheduling commitments as drummer for Relient K. Judge also filled in for Brian Leppke of metalcore band Bleeding Through when he was unable to turn up for the Thrash and Burn tour in May.

[23] In December 2011, Ryan Helm announced that he would be leaving Demon Hunter to concentrate on his solo project, Damien Deadson.

"[24] In January 2012, it was announced on the Solid State Records website that Jeremiah Scott, bassist for The Showdown, had joined the band in the position of rhythm guitar.

[33] Demon Hunter officially released their eighth studio album, Outlive, on Solid State Records on March 31, 2017.

[45] On February 10, 2023, the band released a b-side from the Exile recording sessions, "The Brink", which had been an exclusive song to Demon Hunter's fan club, The Blessed Resistance, in 2022.

[51] On February 7th, 2025, alternative rock band Set the Sun released a collaboration with Demon Hunter titled "Falling Apart".

"[53] Ryan Clark claimed, "When we officially started we wanted to be very bold about it, we didn't see any purpose of just beating around the bush.

A Navy SEAL who claimed to have killed Bin Laden was quoted as saying "'[W]e stopped using [Metallica's] music, and then a band called Demon Hunter got in touch and said, "We're all about promoting what you do."

'"[56][57][58] The day after the story broke, Demon Hunter addressed the situation by saying they approved US servicemen wearing their patch, but they didn't volunteer their music, nor did they have any knowledge of it being used for interrogations.