The Watchtower functioned as a troop transport shuttle utilized by the Imperial Navy amidst the Galactic Civil War, which was waged against the Alliance to Restore the Republic. After the Death Star's annihilation during the Battle of Yavin, the starship was dispatched to the Devastator, an Imperial-class Star Destroyer, to gather surviving Death Star staff members who required reassignment. Pilot Thane Kyrell was moved to the Watchtower for relocation to the planet Kerev Doi. Upon embarking, he bid farewell to his love Ciena Ree with a kiss, which prompted whistles from multiple Imperial officers present on the vessel. On Kerev Doi, the shuttle was used to project power while transporting the officials in charge of exploiting the planet's dishonest financial institutions. Kyrell was assigned the duty of piloting TIE/ln space superiority starfighters at low altitudes over regions requiring coercion, but he ultimately deserted the Empire and escaped from Kerev Doi.
The canon novel Lost Stars, authored by Claudia Gray and published in 2015, marked the initial appearance of the Watchtower.