Under the exclusive order of James McCloud, the Great Fox (along with ROB 64 as the main operations pilot and essentially ship "voice") was developed and constructed by Arspace Dynamics. The Great Fox was originally to serve the Star Fox team as a carrier & repair facility for the team's Arwings, as well as acting in a logistical capacity by transferring supplies to the combat zones when needed. The customised specifications and technical capabilities of the mothership made it so expensive, James had to take out an 80-year low interest mortgage to ensure the ship was properly built to it's maximum potential. Since James never managed to use this mothership himself, due to disappearing and presumably perishing on Venom before the ship was completed, the Great Fox was still relatively new when James' only son Fox took ownership of the ship to re-form the Star Fox Team following his father's apparent death, and taking ownership of the ship debts too.
As the flagship and mobile HQ of the newly reformed Star Fox Team, the Great Fox played a major role in the Cornerian war against Andross's Empire in the evil emperor's conquest of the entire Lylat System.
The ship's first major assignment was when ROB received General Pepper's urgent distress call, requesting the Star Fox team's aid in breaking off the invasion of Corneria by Andross's overwhelming space fleets, and then recapturing the occupied territories of the Lylat System, and ultimately invading Venom itself, where Andross would need to be defeated to end the war.
Due to the vast numbers of asteroids making a clear flight path nearly impossible, the Great Fox moved up in front of the four Arwings, blasting some of the free floating space rocks to make a more clear head start.
As the Missions on Titania and Macbeth required the use of the Landmaster tank to stay close to the ground, the Great Fox launched the tank from the front bay so Fox could follow ROB's directions in the search for the recently lost Slippy after he crash landed and was captured by the Goras, and to closely follow the Forever Train before it could reach the supply depot. After the Mission on Macbeth was achieved, the Great Fox flew low enough to bring Fox's Landmaster back in, but while on Titania, he used the tanks hover jets to enter the mothership through the back door.
As the Mission required the use of Slippy's experimental attack submarine, the Great Fox complied with Fox's orders to launch the Blue-Marine into the Aquas Ocean, by submerging itself halfway into the sea to drop off the submarine from the front hangar.
In the most important role it played in the war, the Great Fox came under a surprise attack from six powerful Copperhead Missiles under guidance from the advanced Invader III fighters in the Sector Z combat zone. Since the Missiles were launched at a short distance at an angled flight path, the Great Fox was unable to defend itself from the sidelines and landed the four Arwings to take out the attackers.
Due to the many battleships creating barricades to prevent the Star Fox team from reaching Venom's air space, after ROB sent out a signal to indicate readiness, the Great Fox moved into position to give cover fire and blast any cruisers to disable their shields and render them even more vulnerable to the Arwings.
After Fox defeated Andross in his palace on Venom, the Great Fox flew back to Corneria with the four Arwings in tow so the victorious Star Fox team could meet with General Pepper. In the midst of the General's promotional proposal and Fox's polite decline, ROB contacted Fox to inform him that the Great Fox were fully prepared to leave, motivating the Star Fox team to head off to their next Mission.
In the years following the defeat of Andross, the Great Fox soon fell into a state of disrepair, due to lack of funds (with freelance work becoming harder to come by) to keep up maintenance. Its exterior armor began to deteriorate, and it's engine power decreased considerably, to the point where the ship was only able to drift with its boosters. Also, the weapon systems ceased to work, as such Fox was unable to count on space support while chasing down and battling the resurrected Andross out in space above Dinosaur Planet, where the Great Fox was orbiting.
With the reward money received by General Pepper for successfully saving Sauria from destruction and the Lylat system from devastation, the Star Fox team were able to do exactly what Peppy had in mind and completely overhaul the worn out Great Fox. It now appeared as a much sleeker and cleaner looking ship, inside and out, and also added new equipment. This included a long-range transfer system that can send Arwings and Landmasters to a planet's surface when needed, though the team's leader Fox McCloud indicated that it had poor targeting systems.
The ship served the team well, allowing Star Fox to appear where needed throughout Lylat during the Aparoid Invasion. Eventually, the Great Fox led a fleet of Cornerian Defense Force warships to the Aparoid Homeworld, where in the conclusion of the battle, a large swarm of Aparoid Crawlers attacked the Great Fox out in space, while the team was trying to gain access to the planet's core. Its systems compromised and, due to the lack of proper weaponry on exposed areas of the ships' hull, it soon fell prey and was infected by the machine-assimilating aliens. Before the Great Fox could be compromised, despite ROB knowing it not survive much longer and would result in their deaths, he did as he was told when Peppy ordered the ship to divert all remaining energy to the main laser cannons and vaporised the entire Aparoid city to clear a straight path towards the Anti-Laser Shield blocking the main entrance to the core. Against the four Arwing pilots pleading him to stay with them, Peppy deliberately ignored them by heroically spearheading the mothership into the shield to allow the four Arwings to get through, but this crashing blow crippled the ship and endangered Peppy and ROB's lives since the shield was undergoing a restoration of itself and would soon return and engulf them in an explosion.
After the Aparoid Homeworld went into meltdown, even though the Great Fox ship was destroyed by the shields restoration and the crew believed to have perished, Slippy managed spot a flashing beacon amidst the wreckage of the Homeworld, revealing that Peppy and ROB escaped at the last moment in the ship's bridge, which could also serve in an escape pod function. The pod, rejoining the team following the destruction of the planet, flew back to Corneria.
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