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rince of Persia: The Two Thrones follows the second ending of Prince of Persia: Warrior Within, in which the Prince kills the Dahaka, essentially saving Kaileena. While on a ship going home to Babylon, the Prince tosses the Amulet of Time overboard. Upon returning to Babylon, he is horrified to find the city is burning and ravaged by war. His ship is attacked and he and Kaileena are thrown overboard, with Kaileena taken prisoner after drifting ashore. After fighting his way through the city, the Prince discovers that as a result of his efforts on the Island of Time to prevent the Sands of Time from being created, the events of Prince of Persia: The Sands of Time never happened, thus, the Vizier was never killed. The Vizier possesses the Dagger of Time, and the magical staff, as well. The Vizier is now in search of the Sands of Time, and has captured the Empress of Time to get them. Just as the Prince finds Kaileena, the Vizier kills her and unleashes the Sands of Time. Then the Vizier transforms into an immortal being by impaling himself with the Dagger of Time, which now contains the Sands of Time. The released Sands of Time also strike the Prince, infecting his open wound and embedding the daggertail into his arm. The Prince breaks free of bondage, and escapes, grabbing the Dagger of Time in the process.

As the Prince travels through the city once again to kill the Vizier, he finds that the Sands of Time have effected his mind. He has essentially been split into two personalities: one which, for the most part, strives to do good, although is fueled by vengeance, and the Dark Prince, manifested by an internal voice that speaks to the Prince. The Dark Prince is a cruel and arrogant being, who throughout the game, attempts to convince the Prince that they are the same person, and that the Prince should strive to serve only himself, using his vengeance as a catalyst for the Prince's emotions. While searching for the Vizier, the Prince encounters Farah, who does not remember him, and is surprised that the Prince knows her name. As the game progresses, the Prince learns more about the nature of the Dark Prince, who is in fact, not a part of the Prince, just the manifestation of the Sands of Time trying to overcome his body and mind. The Prince eventually starts to ignore the Dark Prince, being inspired by Farah to be fueled by compassion for his people who are suffering, rather than be fueled by vengeance for the Vizier.

When the Prince finally finds the Vizier, he casts him into a dried well, where the indwelling Dark Prince tries more aggressively to take control. The Prince eventually finds the dead body of his father, who he had hoped to reconcile with, and is forced to face his wrong actions. By accepting the consequences of what he has done, he silences the Dark Prince, seemingly in permanence. The Prince escapes the well, and once again confronts the Vizier, who he kills by impaling him with the Dagger of Time. Kaileena appears to the Prince and cleanses him of his infection by the Sands of Time, and all his wounds. As the Prince leans down to reach for his father's crown, he is confronted by the Dark Prince, who draws the Prince into his mind, where the two struggle for control. The Prince eventually realizes that fighting the Dark Prince will only intensify his anger, thus feeding the Dark Prince, so he decides to simply ignore the Dark Prince, who is eventually silenced, starved of anger and aggression. The Prince then awakens in Farah's embrace.