The game starts out with a recap, detailing Gabriel Belmont's transformation into Dracula and his encounters with his son, Trevor, whom he kills and subsequently resurrects, and grandson, Simon. The game starts proper with knights attacking Dracula's castle. He swiftly dispatches all of them before being confronted by the revived Trevor, now known as Alucard.

A thousand years have passed and Dracula awakens in a cathedral in modern times, weak from starvation and with no memory of the circumstances that led him there. He is warned by his former enemy, Zobek , of the return of Satan, who until then was deterred from doing so by Dracula himself. Zobek offers him the Vampire Killer, the only weapon capable of ending his cursed existence, in exchange for him vanquishing the people trying to bring Satan back, his acolytes. The key to him regaining his power lies in his castle, which the cursed blood that kept it alive for centuries attempts to deter Dracula of his quest. Throughout his journey, Dracula is aided by various allies, including Zobek's bodyguard and specters of his deceased wife Marie and a younger Trevor. He also encounters the Brotherhood of Light and its current leader, Victor Belmont .

Having destroyed two of the acolytes and tracked down the third, Dracula prepares to ambush him but is stopped by the bodyguard, flashbacking to his last encounter with Alucard. It is revealed that centuries ago, Alucard had come to Dracula with a plan to destroy both Zobek and Satan, using his sword, the Crissaegrim, on him to induce a deep sleep and thus setting the current events into motion. The truth now known, the bodyguard reveals himself to be Alucard. Zobek discovers their treachery and angrily confronts them both. Dracula kills him just as the third acolyte summons Satan, who proceeds to summon a flying monster to destroy the human world. Dracula and Alucard are able to kill the beast, only for Satan to possess the latter, forcing father and son to battle. Dracula gains the upper hand and prepares to stake Alucard with the Vampire Killer, despite Satan's insistence that he would not and forcing him to vacate the body. Having anticipated this, Dracula kills Satan once and for all while saving his son. Dracula then destroys the Mirror of Fate and walks back inside his cathedral with Alucard as the sun rises on the city.

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