Upon hearing that a rebel cell was causing trouble on Lothal in the face of local Imperials, Tarkin decided to take the situation in his own hands. Kanan Jarrus, leader of the Ghost Crew and Jedi in hiding, was captured. The prisoner was taken on board the Sovereign, where he was tortured by The Grand Inquisitor. When it appeared that Kanan was too resistant to the mind probe and refused to talk, the Sovereign set course for the Mustafar System, where the rebel would be further interrogated.
However, the rebels soon came to Kanan's rescue. They stole a Gozanti-class Crusier from a Lothal TIE Fighter airfield, which allowed them to board the Sovereign. Kanan's apprentice, Ezra Bridger, managed to free his master. When they tried to escape through the engine room, they encountered the Inquisitor, and they all engaged in a fierce lightsaber duel. Ultimately, Kanan had gotten the upper hand. The Inquisitor plummeted from the room's central platform, but the remains of his lightsaber fell in the Star Destroyer's engines, causing them to overheat. It started a chain reaction of explosions and the Sovereign, with its stabilizers and propulsion systems disabled, was pulled into the gravity well of Mustafar and exploded. The Grand Inquisitor perished in this ship, but Tarkin, Kassius Konstantine and at least two of their men, however, had managed to evacuate the ship before it was too late.
- "The Siege of Lothal" (Indirect mention only)
- "Secret Cargo" (Indirect mention only)
- The Sovereign first appeared in the Star Wars novel, Tarkin.
- After the Sovereign was destroyed, Tarkin took command of a second flagship, the Executrix.
- The Sovereign is the third Imperial Star Destroyer named to appear in Star Wars Rebels and the first to be destroyed by the Rebels.