The film is set in early 19th century Styria and opens with an atmospheric pre-credits sequence featuring a beautiful blonde (Kirsten Lindholm) in a diaphanous gown materialising from a misty graveyard. Encountering the Baron Hartog (Douglas Wilmer), a vampire hunter out to avenge the death of his sister, the girl is revealed as a vampire when her breast is seared by his crucifix. Baring her fangs to attack the Baron, she is swiftly decapitated.

The main story then begins with a sultry dark-haired lady leaving her daughter Marcilla (Pitt) in the care of General von Spielsdorf (Cushing) and his family at their Styrian mansion. Marcilla quickly befriends the General’s daughter, Laura (Steele). Laura suffers nightmares that she is being attacked, and her health deteriorates until she expires. Marcilla vanishes from the General’s home.

Faking a carriage break-down, Mircalla’s mother leaves her (now using the alias Carmilla) at the residence of a Mr Morton. Here, Carmilla befriends and seduces Morton’s daughter Emma (Smith) but her need to feed overcomes her emotional attachment and Emma too begins to fade. Emma has nightmares of a being pierced over the heart, and her breast shows tiny wounds. Emma’s governess Madame Perradon (Kate O’Mara) also falls victim to Carmilla’s erotic blandishments and becomes her willing tool. Some in the household, the Butler and a Doctor, suspect what might be happening, especially in the wake of several local girls suddenly dying. But Carmilla kills each one. All the while, a mysterious Man in Black (clearly also a vampire) watches events from a distance, smiling (his presence is never explained).

After Carmilla kills the Butler, having convinced him that Madame Perradon is a vampire then persuaded him (for some reason) to remove the garlic protecting Emma, Carmilla goes to Emma’s bedroom. She says she must go away, but is taking Emma with her. A desperate and sick Madame begs Carmilla to take her with her. Carmilla kills her, in front of a horrified Emma. Emma is barely rescued by a young man named Carl (Jon Finch) who fashions a makeshift cross from his dagger. Carmilla flees to her nearby ancestral castle, now a ruin.

All this coincides with the arrival of the General, who brings with him a now-aged Baron Hartog. They find Carmilla’s grave, where she sleeps. Her eyes open, and interestingly enough she makes no move to defend herself. The General lifts a stake–and back in her bedchamber Emma screams “No!”–then drives it into Carmilla’s heart. He then cuts off her head. Carmilla’s portrait on the wall decays, showing now a fanged skeleton instead of a beautiful young woman.