The Infinite Ocean lies polluted, setting a grim backdrop as the Trix descend to seize power at the Emperor's underwater throne, while the Winx prepare to guide the fresh-faced fairies at Alfea College. During the welcoming ceremony, the group reflects on the myriad talents hidden within every fairy, hinting at the deeper powers they may one day unleash. Afterward, Bloom leaves for her hometown Gardenia with her pet rabbit Kiko to spend a day with her fiancé, Sky, a simple moment that contrasts with the dangers growing beneath the waves.
In the depths of the Infinite Ocean, the Trix attempt to seize the throne but end up summoning the nymph Politea instead. A fierce battle follows, and they learn that the throne answers only to the true emperor, Tritannus. A dangerous deal is struck: to restore Tritannus from Oblivion they must use the life force of a young princess, and in return Politea will gain the mystical Pearl of the Deep. The Trix push ahead, willing to risk everything to reclaim power and influence.
The danger escalates when the Trix reach Gardenia and confront Bloom and Sky. Bloom fights valiantly, and the pair manage to escape, but Kiko is captured. Bloom attempts a dangerous rescue, is knocked unconscious, and the Trix take Kiko to the Infinite Ocean. Bloom’s fate tightens the suspense as she is bound to the Emperor’s Throne while the Trix and Politea regroup. Icy lends a chilling assist to the awakening of Tritannus, who regains his memory and learns more about the Pearl’s whereabouts from Politea. With Tritannus now on the throne, he seals all gateways to the Infinite Ocean, forcing the heroes to seek another path toward Omnia where the Pearl is said to be hidden.
Back at Alfea, Bloom’s friends rally to help [Sky] embark on this perilous mission. They discover that all ocean gateways have been sealed except for the dangerous Oblivion portal, which threads the group into a strange and dangerous dimension. The Winx venture through the Oblivion, and Sky awakens in an empty chamber to a dark illusion of himself that accuses him of abandoning Bloom. Realizing the danger, the team rouses themselves and uses a convergence spell to break free, pulling together to push back against the Oblivion’s grip.
The pursuit leads the group back toward the Emperor’s Throne, where the Winx confront Politea once more. Bloom regains consciousness and urges the team toward Omnia, where the Pearl was hidden in the Coral Barrier. They arrive to face the Trix and Tritannus, and Tritannus seizes the Pearl, only for Politea to appear and snatch it away from him. She sits on the Throne, revealing that she deceived the Trix and has no intention of honoring their deal. The Trix attempt to resist, but Politea hypnotizes them and Tritannus, gaining control of the situation.
Sky manages to break free from the throne’s hold, but the price is steep, and he dies in the struggle, leaving Bloom to mourn a profound loss. Domino's Selkie Serena then intervenes, snatching the Pearl from Politea’s grasp and delivering it to the Winx. With the Pearl secured, the Winx unleash a final convergence spell to defeat Politea, and Omnia uses the same magic to heal Sky, offering a glimmer of hope amidst the devastation.
In the aftermath, Sky awakens at Alfea and asks what happened to the Trix and Tritannus. The Winx recount the truth: the Trix fled, Tritannus is once again banished to the Oblivion, and the Pearl rests where it belongs. In a closing moment of reconciliation and relief, Sky shares a kiss with Bloom, while Kiko returns with a playful ice cream for Sky, a small reminder of brighter days ahead.
