Despair-class hunter-killers were present at the Battle of Janjur Qom. At the close of the Forerunner-Flood war, multiple Despair-class fighters were stationed at Requiem in defense of the shield world. Several Despair-class fighters saw action against the rogue Contender-class artificial intelligence Mendicant Bias. After the firing of the Halo Array, some of the Despair-class fighters were moved to shield worlds and Halo installations. At least one Despair-class hunter-killer was moved to Installation 00 by the Librarian.
In May 2559, a Despair-class fighter's design seed was found and reactivated by Colony's Huragok, with the Banished planning to use the fighter to destroy the UNSC Spirit of Fire. The Banished managed to establish a cloaking shield around the fighter to protect it from detection as the ship prepared for launch, but recon drones noticed the cloaking shield and the ODST squad Sunray 1-1 was sent to investigate. Despite heavy Banished and Sentinel resistance, the UNSC forces managed to take over five Forerunner Control Towers in the area and deactivate the cloaking shield, causing a Retriever Sentinel to attack. Once the Retriever was destroyed, the Spirit of Fire discovered the hidden Forerunner ship.
With the Banished's Huragok hacking the Ark's local systems to prep the ship for launch, an attempt was made to send in a Condor gunship to destroy the fighter without success. Instead, Sunray 1-1 led an assault on the fighter. While it was originally believed that the Banished intended to use the fighter to get reinforcements in lieu of the destroyed Enduring Conviction, it was quickly determined that the fighter was going to be launched on a collision course with the Spirit of Fire itself with a direct hit being enough to destroy the human ship. Spotting four charging columns connected to the ship, the UNSC forces, fighting through heavy Banished and Sentinel defenses, assaulted the columns' control pads, using Colossus to destroy them, delaying the ship's launch each time one was destroyed. Finally, with the charging columns destroyed and the Banished forces in the area defeated, Quinn was able to use the control terminal near the fighter to shut it down. Though the Banished sent in a Hunter Captain supported by Goliaths, the UNSC was able to clear out the Banished forces. To ensure the Banished could not try to use the ship again, Sunray 1-1 dropped satchel charges from Hornets while Quinn lowered the ship into the ground. The charges destroyed the Despair-class fighter, keeping both the Banished and the UNSC from using it.
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