Bloom, [Letizia Ciampa], and her friends Stella, [Perla Liberatori], Flora, [Ilaria Latini], Musa, [Gemma Donati], Tecna, [Domitilla D'Amico], and Aisha, [Laura Lenghi], search for Bloom's birth parents, King Oritel and Queen Marion. They seek the help of Hagen, [Rodolfo Bianchi], the blacksmith who forged Oritel's powerful sword. Sneaking into Hagen's castle, they are mistaken for intruders. Faragonda, [Emanuela Rossi], an old friend of Hagen's, intervenes, and they return to Alfea empty-handed. Despite Bloom's plea for assistance, Hagen confesses his inability to help, leaving Bloom feeling guilty for her friends' futile efforts. She flees in tears to avoid confronting them.
Most of the third-year fairies at Alfea, including the Winx (except Bloom), graduate and become guardian fairies of their home planets after obtaining their Enchantix powers. Bloom, with her incomplete powers, stays behind, watched over by Sky, [Marco Vivio], who consoles her and encourages her to continue her quest despite Hagen's discouragement. Their tender moment is interrupted by the sudden arrival of a mysterious girl. The following day, Bloom departs for Earth to stay with her adoptive parents. Despite appearing content, her discomfort on Earth is evident to Mike and Vanessa, who recognize her true belonging in the Magical Dimension. That night, Bloom has a dream of her sister Daphne, who provides hope by revealing that their parents are still alive and shares vital information about the Book of Fate.
The next morning, Bloom is surprised by her friends gathering at her house to celebrate her nineteenth birthday. United, they agree to support Bloom's plan, reinforcing their unbreakable bond of friendship. Bloom's renewed hope triggers the activation of Oritel's sword, drawing attention from the Obsidian Circle. Troubled by this, the three Ancestral Witches employ Mandragora to investigate and eliminate the source.
Meanwhile, the team journeys to Domino, guided by Daphne's mask and memories. Upon reaching the mountain where the Book of Fate is hidden, they encounter the Roc, a mystical guardian of the library. A mishap with the Specialists awakens the Roc, causing chaos, but the girls ultimately manage to safely land the creature, ensuring their progress continues.
Inside the library, Bloom and her friends meet Bartelby, Oritel's spirit scribe, who reveals the Book of Fate. They learn that Bloom's parents were part of the Company of Light, fighting against the Ancestral Witches. However, crucial pages detailing their fate are missing. Bartelby prophesies the salvation of Domino by six legendary warriors and the freeing of Oritel's sword by a king without a crown. Celebrating this revelation, Riven falls under Mandragora's control.
Alfea is then attacked by Mandragora, who gains insight into Bloom before vanishing. After restoring Alfea, the group heads to Pixie Village in search of a way into the Obsidian Circle. Guided by Lockette, they approach the gateway. Mandragora intervenes, pitting Riven against Sky and endangering Musa.
The girls are forced to face their worst fears, and Bloom sees a vision of what happened to her birth parents: Oritel was pulled into the Obsidian Circle by the Ancestral Witches while Marion absorbed herself into the sword in order to be with him. To Bloom's horror, she sees her father frozen in stone, the same fate for all inhabitants of her planet. All the fairies then wake up from their trances, only to come face-to-face with the Ancestral Witches, who severely weaken the Winx except Bloom. They force Bloom to make a choice between destroying the sword and saving her adoptive parents or taking the sword and letting Mandragora kill them, as seen in an image. Luckily, Bloom sees through the illusion and places her trust in the boys, while they are still fighting Mandragora, unleashing the power of the Dragon Flame.
Outside, Riven recalls all what he and Musa have been through together. Regaining his sanity, he lifts her up and they kiss. Meanwhile, chasing after Mandragora, Sky arrives moments later to aid a struggling Bloom and takes the sword, but supposedly dies, as only a king can wield the sword.
Eventually Bloom's Dragon Flame also succumbs under the darkness of the Obsidian Circle and is ready to give up when Daphne reminds her that she is not alone. She puts on the mask, and Daphne joins with her to destroy the Ancestral Witches. However, Mandragora returns and the Ancestral Witches use her body as a host and begin to strangle Bloom to death, but Sky reawakens and stabs Mandragora with Oritel's sword, allowing Bloom to use the power of the Dragon Flame on Mandragora, destroying both her and the entire Obsidian Circle, completing her Enchantix powers and freeing everyone. Sky explains that he is now the king of Eraklyon, and his coronation was the night he left Bloom at Alfea. With Domino restored to its former glory, Oritel is freed from stone, Marion is released from the sword, and Bloom reunites with her birth parents at last.
At a party afterwards, Oritel and Marion promise Bloom that they will never leave her again. Mike and Vanessa are also there and are greeted by a hug from Bloom. Oritel begins the traditional dad-daughter dance, but lets Bloom dance with Sky, who proposes to her. She delightfully accepts, and as they kiss, Bartelby appears by the Book of Fate, telling the audience that the prophecy has been fulfilled; Bloom is now a guardian fairy and there is a new Company of Light - the Winx.
In the final scene, it is revealed the Ancestral Witches have not been destroyed by the Dragon Flame; instead, their spirits were freed with the destruction of the Obsidian Circle and are finding new hosts to take over and destroy the Winx. They are shown with their direct descendants, the Trix, cackling madly. This is a cliffhanger leading to the second film.
