The story opens in a flashback sequence to the year 1202 AD. An army of medieval warriors arrives at a ravaged village, led by the three vampire elders: Marcus Corvinus, Viktor, and Amelia, followed by an army of the first Death Dealers. Viktor orders his troops to quickly burn the corpses of the slain villagers, but before the task is completed, the bodies awake and transform into werewolves. A bloody battle erupts, and Viktor orders Marcus to retreat. Viktor and Amelia take the rest of their troops into the woods, where they capture Marcus's brother William Corvinus, the first and most powerful werewolf. Marcus returns and angrily demands that William be turned over to his care. Viktor refuses, and orders instead that William will be imprisoned in a secret location forever.
The story then continues the present-day timeline, starting immediately after the events of the previous movie. Selene and Michael take shelter in a vampire safe house which appears to be in Hungary. Selene warns Michael that he can only feed on cloned blood, and that she needs to return to the mansion alone to keep Kraven from killing Marcus. What she doesn't realize is that Singe's blood had awakened Marcus. Marcus breaks out of the sarcophagus on his own and wipes out the entire remnant of Kraven's men, killing Kraven last as vengeance for Kraven's treachery. He learns of Kraven's treachery and the course of previous events by drinking Kraven's blood.
Selene begins to head out on her way back to the mansion, but witnesses what she deduces to be Marcus flying overhead, possibly in pursuit of her. Michael ignores her warnings and tries to order some fish at a restaurant and has a strong negative reaction to the food. The police and the media believe that Michael is a wanted fugitive, and the police, upon seeing his face on the TV screen, immediately recognize him. He begs for them to stay away, but they attack anyway. He rushes away to avoid the temptation to prey on them. They fire rounds at him, but Selene intervenes and quickly knocks out the police.
Marcus finds Selene and Michael. Selene desperately attempts to defend her actions, and Marcus blows off her comments about Viktor, agreeing that Viktor got what he deserved. He does argue that he believes Selene might be hiding something, and attacks her; Michael intervenes and protects her. Marcus tries and fails to get hold of a pendant the two have in their possession. They hijack a truck and escape from Marcus, but he vows to get his fangs on Selene's blood memories one way or another. The two seek refuge in an abandoned warehouse, where they then have passionate sex.
Lorenz Macaro, an elderly and imposing man, sends in a team of "Cleaners" to investigate the finds of all the dead bodies from the first movie. When Macaro examines Viktor's body, and finds a metal disk attached to his ribcage, just below the skin of his chest. Macaro fears the worst as he hears that Marcus' body was not amongst those found at the mansion.
Michael and Selene then set out to solve the mystery of the pendant that Marcus wanted from them so badly. Selene can recall that she'd seen it before as a child, but knew not its significance. She decides they must try to travel to Andreas Tanis' hideout for answers, as he is the exiled historian who could help them out. They arrive to find that Tanis had been secretly involved in weapons trade with Lycans and forces him to tell them as much as he can.
He reveals that Marcus, not Viktor, was the first vampire. One of the three sons of Alexander Corvinus, he was bitten by a bat, and became a vampire; his twin brother, William Corvinus, was bitten by a wolf and became a Lycan. Unlike later Lycans, William, and the Lycans created by him, are entirely animal, unable to take human form again. When William ran amok, Marcus approached Viktor, a warlord, as he was dying of old age, and offered him a deal: to turn him and his army into immortal vampires, in exchange for his help in tracking down and stopping William. Marcus intended to capture his brother and tame him; Viktor had different plans and orders William locked away forever. As time went on, Viktor came to dominate the vampire coven, and was falsely regarded as the first vampire. But Viktor was afraid to kill either Marcus or William, as Marcus had told him that doing so would lead to the immediate extinction of all the vampires or Lycans.
Selene's father is revealed to have been the architect who built William's prison; the pendant is one half of its key, the other half being the disk that Macaro took from Viktor's chest. When Lucian escaped captivity and took the pendant with him, Viktor killed Selene's father and family. Selene's latent memories from her childhood are the map to finding the prison. Tanis then arranges a meeting between Selene, Michael, and "someone who could help stop Marcus." After they leave, Marcus arrives at the Monastery and questions Tanis, biting him, absorbing his memories, and killing him.
Selene and Michael drive to a dock and are taken to Macaro, whom Selene realizes is actually Alexander Corvinus. Since his sons turned, he has devoted his life to containing the vampire-lycan war, keeping it from escalating over to the mortal world. But despite Selene's entreaties, he refuses to help kill his own son, no matter what Marcus has become. Their debate is broken when Marcus attacks the boat. He and Michael fight, and Marcus rams Michael's body down on a wooden stake, impaling and seemingly killing him. Taking the pendant, Marcus then grabs Selene and pins her, taking her blood and finding the location to William's hidden location.
In the ship's cabin, Marcus confronts his father. Alexander fails to convince Marcus to back down from his quest to free William. Marcus rants and muses becoming a god, and mortally wounds Alexander to get the second part to William's key (the disk that was attached to Viktor's ribcage). The Cleaners take Selene to Alexander, who begs her to take some of his blood for her own sake, promising it will make her "the future." She drinks it and demands that Michael's body stay with her.
The Cleaners and Selene, with Michael in a body bag, arrive by helicopter too late, and find that Marcus has already freed William. A violent battle ensues, and the Cleaners are transformed into first-generation Lycans, leaving Selene alone to defend herself. Michael suddenly regenerates and jumps from the helicopter to help her just as Marcus manages to shift the stone door that he becomes trapped behind, and joins the fight. Marcus, seeing the helicopter above, pulls on a rope it is attached to, bringing the entire machine down upon them all.
Selene battles Marcus while Michael fights with William. Marcus is distracted when Michael tears off the top of William's head. In a rage, he impales Selene through the gut with one of his wing spikes. He tells her Viktor should have killed her along with her family. Selene, furious, pulls out the talon, breaks it off, and rams it up into Marcus's head. She sends him flying into the still moving helicopter blades, killing him. Selene and Michael find themselves the only monstrous beings left alive in the caverns and are amazed to discover that sunlight no longer affects her. Selene narrates that she fears dark days are ahead, as the lines between the species have become blurred, but states that she is at least optimistic that she won't have to face the future alone.
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