The Eternal Flagship functioned as the primary command vessel, or flagship, of the Eternal Fleet. This capital ship was under the authority of Arcann, who held the titles of Prince and later Emperor of the Eternal Empire.
Emperor Valkorion, Arcann's father, ordered the construction of the Eternal Flagship during the zenith of his power. Serving as the vanguard of the Eternal Fleet, it stood as a potent representation of the might and grandeur of Zakuul. Unlike the rest of the fleet, which was controlled by GEMINI droid captains, the Eternal Flagship was manned by the most capable and devoted humans within the empire.

Notably, Arcann and Thexan were transported into battle aboard the Eternal Flagship during their conquest of the Core Worlds. The flagship swiftly disabled Balmorra's planetary defense systems, enabling the twin princes to seize the planet's weapon manufacturing facilities intact. In recognition of this significant achievement, Emperor Valkorion himself bestowed upon the flagship's crew Zakuul's highest distinction, the Medal of Eternal Valor.
Following the space battle against the combined forces of the Sith Empire and the Galactic Republic, Prince Arcann of the Eternal Empire utilized the vessel to transport prisoners to his father.
In 3631 BBY, Arcann, aboard his flagship, led a substantial portion of the Eternal Fleet to intercept the Outlander as they attempted to commandeer a solitary Eternal Fleet warship. Upon their arrival and subsequent attack, the Gravestone managed to escape into hyperspace. Consequently, Arcann's flagship relinquished control over all Eternal Fleet vessels beyond their immediate sector, as SCORPIO had assumed command of the remaining ships.

SCORPIO then provided Arcann with intelligence regarding the location of Odessen, the Alliance's primary base. As Arcann's fleet neared Odessen, the Alliance Commander, accompanied by their closest allies, approached in the Gravestone. After clearing a path, the Outlander, along with Lana Beniko and Senya Tirall, boarded the flagship. The Outlander became separated from their team when SCORPIO revealed her complete control over the fleet, initiating an attack on the flagship. The Outlander fought their way to Arcann and defeated him using the combined power of Valkorion, Satele Shan, and Darth Marr. However, before the battle could conclude, a section of the roof collapsed on Arcann. As the Outlander headed towards a fighter in the hangar, Senya Tirall rescued her son from the wreckage, only to be confronted and nearly killed by Vaylin. As Vaylin lunged at her mother, Arcann awoke and pushed her back, mirroring their brother's earlier intervention that prevented Arcann from killing Valkorion.
Senya escaped to a shuttle in the hangar with the wounded Arcann. The Outlander faced a critical decision regarding their fate, with Koth Vortena urging them to destroy the shuttle before it could jump to hyperspace. The remnants of Arcann's Fleet regrouped for a coordinated assault of an unspecified nature, but the Gravestone fired, disrupting and obliterating them. The ensuing explosion nearly annihilated the Outlander, their crew, and the Gravestone.
During her reign as Empress, Vaylin employed a similar vessel as her flagship during her mission to Nathema and the Assault on Odessen.