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The story features seventeen-year-old Dhampir (half-human, half-vampire) guardian-in-training Rose Hathaway (Zoey Deutch), and her royal Moroi (the peaceful, mortal vampires) best friend Lissa Dragomir (Lucy Fry) living discreetly within our world, having escaped from their boarding school St. Vladimir's Academy one year prior to the beginning of the story, following a series of warnings and threats. They are soon dragged back to the Academy in Montana and rediscover the dangerous hierarchy within it, along with lies, rumors and secrets, both struggling to fit in to the school politics. Rose starts to form an attraction to her Russian Dhampir mentor and fellow Guardian, Dimitri Belikov (Danila Kozlovsky).
Mysterious messages threatening Lissa start to appear (messages written on the wall in blood and an exploding memorial to her family in the school church), but it turns out to be the work of classmate Mia Rinaldi (Sami Gayle), who once dated Lissa's brother Andre, a playboy who enjoyed non-committal relationships. Mia was clingy and focused her hatred towards Lissa as the only surviving member of the Dragomir line. Manipulating two other students using sex, she persuaded them to help her in her fear tactics against Lissa. A Moroi named Christian Ozera (Dominic Sherwood), who is viewed poorly by his peers because his parents became Strigoi (the evil, undead vampires of legend, which Moroi become if they completely drain their victims of blood), tries to romance Lissa but Rose manages to keep him away by lying to both Lissa and Christian. Rose also discovers that Lissa has the same rare power that the founder of their school St. Vladimir had, that of Spirit, a power which enables the caster to heal ailments, and save the dying. At the same time as Mia and her two compatriots have been leaving her nasty notes threatening her safety dead animals have been popping up wherever Lissa goes, including her beloved cat Oscar. At the Equinox Dance, Rose confronts Mia, believing she is responsible for all the dead animals and the notes. Mia, however, is horrified because she loves cats and gave Oscar treats. Soon, Lissa is kidnapped and Rose, Dimitri, and Christian go to save her.
The Moroi responsible for Lissa's kidnapping and the threats against her is Victor Dashkov (Gabriel Byrne), a previous candidate for the throne, who has contracted a disease that leaves him too feeble for the job. He wants to use Lissa to cure himself, even knowing that the cure would cost her her life as continued healing would eventually take its toll on her. Once captured and placed in the secure cells beneath the school, Victor explains to Rose that the reason why she bonded to Lissa (and is therefore sometimes able to see through her eyes) is because she was "shadow-kissed", having been brought back to life by Lissa's magic. While they are talking, Victor's daughter Natalie (Sarah Hyland) - who befriended both Lissa and Rose and was a very insecure, almost invisible, student at the school - is enacting the tools of his escape having turned Strigoi by draining her crush to death, instead of losing her virginity to him. Rose helps Dimitri kill Natalie and detain Victor.
During a speech by vampire Queen Tatiana Ivashkov (Joely Richardson), Lissa steps in and gives a speech of her own, announcing that Spirit is her type of magic, and that it is thanks to Rose (who will help keep her from straying from the person she truly is) that she can master it. Rose then goes outside to meet Dimitri and ask about his feelings for her. He states that he can't love her because if there was any danger between Rose and Lissa he wouldn't save Lissa, and that he would save her. Rose gives Dimirti a kiss on the cheek and walks back to the academy. The scene then shifts to a mountain cave not too far from the academy, where a massive army of Strigoi reside, among them being Miss Karp, a teacher with Spirit Magic that turn herself Strigoi after being driven insane by her magic. She says it will be time soon.