Griffin was one of the three CSN carriers that took part in Operation Menelaus. It was severely damaged during the mission when an Imperial starfighter crash landed on its flight deck. It then suffered a mis-jump upon attempting to return to Spirit and was eventually engaged in a battle with Ifrit.

As of June 2617, the carrier was taken out of service and consigned to several months in dry-dock for repairs.

After returning from the Phylent system, Griffin spent six months in dry dock, undergoing repairs at Spirit.

In late 2617, Elliott Parks took Griffin to the Coyote system to aid in the rescue of the White Knights and the salvaging of the ATAFs from the bottom of the Tanis Sea. Amanda Jenkins was initially against the idea of taking the carrier, as it had been out of action ever since the failed Operation Menelaus, and she did not wish for the CSN to lose two carriers in one day.

Griffin played a part in the battle of Coyote, joining Leviathan, Talos and a host of other UNF forces around the planet Mythos. It became the prime target of Dragon when the Pandoran forces summoned the ship into the system, to further aid them in their battle. Griffin was given a reprieve from becoming the latest victim of the battleship's anti-matter cannon when the TSBs aboard Grendel's Mother detonated and the opposing sides were forced to move to minimum safe distance.

Griffin continued to serve the CSN under the command of Elliott Parks throughout the Pandoran campaign, battle the enemy mostly on the frontline.

During phase two of Black Widow, the carrier was heavily damaged in a direct attack from Chimera, after Parks had moved the carrier up the field, close to Phoenix, in order to destroy the allied super carrier before it fell into enemy hands. Chimera directed a plasma accelerator charge against Griffin, shattering part of the carrier's frontal viewport and spacing some of the crew. Griffin immediately jumped to the Gabriel system.

In late 2624, Griffin formed part of the fleet that Parks took to Mitikas space, in order to hunt down Zackaria. The carrier was involved in a brief skirmish in the Krasst system, but otherwise faced no major opposition.

Following Parks' death, Amanda Jenkins took over command of Griffin for the final battle for the Solar System. The carrier suffered a great deal of damage, but survived the battle.