The ponies of Equestria prepare for their first Friendship Festival, which is overseen by Princess Twilight Sparkle in Canterlot. The festivities are interrupted by an invasion of monstrous storm creatures commanded by the broken-horned unicorn Tempest Shadow, who uses magical obsidian orbs to petrify Twilight’s fellow princesses; Princess Celestia unsuccessfully urges Princess Luna to seek help south of Equestria, uttering “the queen of the hippo” before being interrupted. Twilight flees the city alongside her five pony friends – Pinkie Pie, Rainbow Dash, Rarity, Applejack, and Fluttershy – and her assistant dragon, Spike, setting out with them in search of the aforementioned “hippos”. Tempest is contacted by her superior, the Storm King, who reminds her to gather all of Equestria’s princesses in order for him to activate his mystical staff with their magic, promising to restore her horn in exchange.
In the desert city of Klugetown, a feline con artist named Capper falsely offers to guide the seven friends to the hippos, secretly intending to sell the ponies to settle a debt to a local criminal. However, he develops a genuine friendship with them after Rarity generously mends his coat. Twilight discovers an atlas in Capper’s manor that reveals the “hippos” to be hippogriffs, exposing Capper’s treachery to the others. When Tempest arrives in pursuit of Twilight, the seven evade her aboard a delivery airship. Tempest interrogates Capper over Twilight’s whereabouts, but he deliberately misdirects Tempest to atone for deceiving the seven.
The airship’s birdlike crew reluctantly allow the seven passage during a lunch break, revealing themselves to be former pirates that have been forced into the Storm King’s service. Rainbow Dash persuades the pirates to defy orders and take the seven to the hippogriffs’ kingdom on Mount Aris, performing a Sonic Rainboom that inadvertently gives their location away to Tempest. Disgruntled by her friends’ carelessness, Twilight single-handedly engineers her group’s escape in a makeshift hot air balloon, leaving Tempest to destroy the ship with the pirates and Capper on board.
The seven reach Mount Aris to find the kingdom deserted. Following a singing voice to a fountain, they are pulled down a whirlpool where the singer, the seapony Princess Skystar, gives them air bubble helmets and takes them to her underwater home of Seaquestria. Princess Skystar identifies her kind as the hippogriffs, transformed by a magic pearl used by her mother, Queen Novo, to hide from the Storm King’s assault; Queen Novo demonstrates by turning the ponies into sea ponies and Spike into a pufferfish. When Queen Novo denies them the pearl to use against the Storm King, Twilight desperately attempts to steal the pearl while letting her oblivious friends socialize with the seaponies as a distraction. Pinkie Pie nearly changes Queen Novo’s mind until Twilight triggers an alarm, prompting the outraged queen to banish the entire group to the surface.
After arguing with her friends over her actions, an ashamed Twilight is abducted by Tempest and brought before the Storm King in Canterlot to have her magic absorbed; Tempest gains Twilight’s sympathy upon divulging how her own friends feared and shunned her for her dangerously unstable magic after she lost her horn in a monster attack as a filly. Meanwhile, Twilight’s friends reunite with Capper, the pirates, and the hippogriff Princess Skystar to infiltrate Canterlot and rescue her. Seeing the group repel his army, the Storm King uses his empowered staff to unleash a tornado on the city, betraying Tempest as well. Twilight saves Tempest from the tornado and reconciles with her friends, working together with them to take the staff from the Storm King and disperse the storm. The Storm King hurls an obsidian orb at the seven in a final effort to reclaim the staff, but Tempest jumps in his way, petrifying them both. The Storm King’s body falls and shatters, while Twilight and her friends use the staff’s magic to revive the petrified ponies and repair the damaged city.
The Friendship Festival resumes, and the ponies celebrate with all of the allies they have made on their adventure. Tempest is convinced by Twilight to join them by using controlled sparks from her still broken horn to provide a fireworks display, happily accepting the friendship of Twilight and her friends