In the months leading up to an event known as The Unholy Masquerade, a documentary crew is granted permission and protection to film a group of vampires living together in a flat in New Zealand. One of the vampires, Viago (Taika Waititi) summons his flatmates Deacon (Jonathan Brugh), Vladislav (Jemaine Clement), and Petyr (Ben Fransham). Petyr, who is the most monstrous of the four, growls at Viago, so he lets him stay in his room.
The other three gather for a meeting. Viago and Vlad chastise Deacon because he hasn't done the dishes in five years. Deacon argues that vampires shouldn't have to do chores.
We learn that Deacon was formerly a Nazi before becoming a vampire. After the Nazis lost the war, he was attacked by a creature that turned him into a vampire, which he later learned was Petyr, who is the oldest of the four at 8000 years old. Deacon is 183, the youngest of the four, and described as a rebellious bad boy younger brother. Vlad, at 862 years old, was considered a tyrant and sexual deviant that enjoyed poking people. His archenemy is another vampire he calls "The Beast".
The vampires go around the streets of Wellington at night for people to prey on. Since they are only able to go out at night, they aren't accustomed to the present day lifestyle. They go to a hotel bar where they meet a human named Jackie (Jackie Van Beek), who acts as Deacon's servant in exchange for the promise to become a vampire and gain immortality. Deacon orders Jackie to find a male and female virgin to bring to the flat. As the other vampires put it, they enjoy drinking virgin blood because it makes them feel cool (in Vlad's words - "it's like eating a sandwich...you'd feel better eating it knowing nobody has fucked it").
Jackie brings her ex-boyfriend Nick (Cori Gonzalez-Macuer) and Katherine (Ethel Robinson), a woman that made fun of Jackie in primary school. They have dinner, where the vampires turn Nick's spaghetti into worms, to his disgust. Viago ends up killing Katherine when he bites into her main artery, causing blood to squirt everywhere. Nick makes a run for it, but Petyr attacks him and turns him into a vampire.
Two months later, Nick has become a member of the flat. He is still getting used to things like flying, drinking blood, and not eating anything that isn't blood. He eats a fry and projectile vomits blood. He joins Viago, Vlad, and Deacon on the streets where he carelessly tells random people that he is a vampire, including one man claiming to be a vampire hunter. Nick also tells his best friend Stu (Stuart Rutherford), who is unfazed by the revelation. The vampires also run into their rivals, the werewolves, led by Anton (Rhys Darby). The werewolves are proper and choose not to swear ("werewolves, not swear-wolves"), but their agitation with the vampires makes them morph slightly.
The vampires hear a screeching sound from the basement. They look to see Petyr on fire, having been exposed to sunlight. Petyr burns to death, and the vampires find another body on the floor of the basement with his head turned backwards. It's the vampire hunter that Nick spoke to. The other three are angry at Nick for indirectly causing Petyr's death. They shame him (walk around him in a circle and point while going "Shame! Shame! Shame!") and banish him from the flat. Deacon also decides to punish Jackie for bringing Nick to them and prolongs their deal.
The vampires receive their invitation to The Unholy Masquerade, but Vlad becomes furious when he learns that the guest of honor will be The Beast. This causes him to age out of stress.
Viago and Deacon go to the party, where other creatures like zombies and witches are in attendance. Nick, Stu, and Jackie are also there. Nick has turned Jackie into a vampire, to Deacon's frustration. Going up to the stage is The Beast, which turns out to be a vampire woman named Pauline (Elena Stejko), Vlad's ex-girlfriend that he named "The Beast" due to their nasty break-up. Pauline notices Stu among everyone else, and the others are forced to admit that he's a human. Furthermore, they deduce that he's a virgin because he works for a software company. The vampires (sans Viago, Deacon, and Nick) get ready to feast on Stu, when Vlad shows up wearing a mask. Pauline calls him an asshole and sics her new boyfriend on him. The two fight, and the boyfriend nearly sucks out Vlad's soul, until Stu impales the boyfriend. He joins Viago, Vlad, Deacon, and Nick as they all flee.
On the run, the gang runs into the werewolves again. The full moon is out, and they all morph into their creature forms. They attack Stu and one of the cameramen, ripping them apart. The other vampires mourn Stu.
Sometime after, Stu shows up at the flat, now a werewolf. He and Anton's werewolf pack become friends with the vampires, with Nick's help. The other vampires have also forgiven Nick.
In time, the vampires adjust to modern life. We see that Viago turned his long lost love into a vampire, and are now finally together forever, and happy, despite her now being in her 90's. (He had planned on doing this 70 years earlier with her, but that plan got sidetracked).
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