The movie begins with a party at Alfea to celebrate the new school year. All of the witches from Cloud Tower are also there. The Trix are there as well, and use this as a means of cover while they try to steal the mystically powerful Compass of Revealed Secrets. However, the Winx Club catch them and the two groups begin battling. While fighting, Darcy sneaks away to steal the Compass of Revealed Secrets from Alfea.
Meanwhile, at her home world of Domino, Bloom is soon overwhelmed by her three maids. After the maids attempt to feed her a live goldfish, she sets it free in an indoor pool. Daphne, Bloom's ghostly and spiritual elder sister, appears and attempts to cheer her up. Afterward, Bloom's parents give her a horse named Peg as a present. While out riding, she finds Sky, so the two go for a ride. Upon returning to the palace, Sky proposes to Bloom.
The Trix report their success in stealing the Compass of Revealed Secrets to the Ancestral Witches. The younger witches then receive their next mission, to use the compass to find Pixie Village, and destroy the Tree of Life's positive magic in the universe.
On planet Eraklyon, Sky tells his father, King Erendor, that Bloom had accepted his proposal. Erendor forbids him. He offers no further explanation, giving Sky a sealed scroll instead.
Later that night, Sky calls Bloom, telling her that they can't get married. Oritel hatches a plan to have Bloom married to someone else which does not sit well with Bloom.
The rest of the Winx find out, through a news show, that Bloom is engaged. Meanwhile, Sky attempts to get into the palace to explain. The Winx arrive and force their way into the palace, and, finding Bloom upset at her maids, ask her about the wedding. Bloom denies knowing anything when Oritel arrives.
Sky, dressed as someone else, arrives. Oritel sees through his disguise before Sky can do any explaining, and bans him from Domino. At this point shoot a fire arrow at Oritel. Sky takes Bloom's horse and leaves. Upset, the Winx leave to Gardenia.
The Winx Club girls' pixies attempt to stop the Trix, but fail and are attacked. The Winx, now on Gardenia, feel this through their bond and pass out. The Trix succeed in destroying the positive half of the Tree's magic strength and energy.
On Earth, the Winx discover the loss of their magical abilities and are able to briefly speak with Faragonda. The pixies have taken refugee at Alfea, and the Winx are told to stay on Earth for the time being.
On Domino, Oritel is furious, until Marion shows him Erendor's confession. While out at a park, Oritel and Marion visit Bloom's adoptive parents, Mike and Vanessa. Mike shows them a few home videos to give them a taste of what her childhood was like, and Oritel decides to talk to Bloom. Meanwhile, Sky calls Bloom and tells her to meet him on Eraklyon. Bloom returns home, but loses her temper at Oritel instead of talking, before the Winx leave again.
At the Tree of Life, the Ancestral Witches discover some positive energy still remains, and remember giving Erendor an hourglass with pollen from the tree inside, so they send the Trix to go get it back.
On Eraklyon, the Winx meet up with the Specialists. The twelve of them board a flying ship that will take them to Avram. During the flight, Sky explains what his father did that caused so much tension. While the Company Of Light was away, in exchange for Eraklyon's safety, Erendor allowed the witches to attack Domino without a fight. The witches then gave him the hourglass, which would serve as protection from the world-shattering dark energy blast should they destroy Domino. After visiting the ruined Avram, Erendor broke the hourglass in remorse and released the Tree's pollen, which took form as a sapling that the Winx now seek.
After a failed physical training session, the Winx and Specialists are attacked by evil hologram versions of themselves, created by the dark magic residue on Avram. Eventually the holograms disappear as a storm tears the ship apart. They manage to land safely on Avram and continue on foot. Back at Eraklyon's palace, the Trix force Erendor to reveal the location of the Tree's magical flower.
The Winx make it to the heart of Avram, but Sky and Bloom are separated from the others. While trying to find their friends, the buildings around them begin to close in. The two fall into the sky, but land safely on another level. The two are reunited each other and Peg as the city begins to fall apart. They manage to ride to safety, finding the Tree's flower.
Meanwhile, the others are attacked by Darcy and Stormy. Oritel arrives and a fight begins. Icy arrives with an unconscious Erendor, but is quickly called away by Belladona, the leader of the Ancestral Witches. Icy takes Erendor to the flower and tosses him into a pit, but he is saved by Oritel. However, Icy blasts the two right back in, but they grab a ledge. While trying to destroy Bloom, Icy accidentally destroys the flower, releasing all of the positive magic at once, causing the Winx to regain all of their magical powers and transform into their Believix forms. Oritel and Erendor are also saved. Peg eats some of the leaves from the tree and sprouts feathered angel wings and a horn, becoming a horned Pegasus.
After attempting to fight, the Trix are punished by having their bodies taken over by the Ancestral Witches,
In the end, the Winx are seen waving to the audience; as they go away, Stella returns back waving, and the Winx take her and fly away, as the credits roll.
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