The ponies of Equestria prepare for their first Friendship Festival, overseen by Princess Twilight Sparkle in Canterlot. The festivities are interrupted by an invasion of monsters led by the tyrannical Storm King, whose enforcer, the broken-horned unicorn Tempest Shadow, uses magical orbs to petrify Twilight's fellow princesses. Princess Celestia gives Princess Luna incomplete instructions to seek help from "the queen of the hippo" before they are both petrified. Twilight flees the city alongside her five pony friends – Pinkie Pie, Rainbow Dash, Rarity, Applejack, and Fluttershy – and her assistant dragon Spike to search for the "hippos". Tempest pursues Twilight under the Storm King's orders to empower his mystical Staff of Sacanas with the princesses' magic in exchange for her horn's restoration.
Twilight's group travel to the desert city of Klugetown, where a feline con artist named Capper offers to escort them, secretly intending to sell them to settle a debt. As Capper begins to develop a genuine friendship with them, Twilight discovers an atlas that reveals the "hippos" to be hippogriffs, exposing Capper's treachery. When Tempest arrives, the group evade Tempest aboard a delivery airship run by birdlike pirates, whom Rainbow Dash persuades to take them to the hippogriffs' kingdom of Mount Aris. In celebration, Rainbow Dash performs a Sonic Rainboom that inadvertently gives their location away to Tempest, forcing the group to reach Mount Aris in a makeshift hot air balloon.
While exploring the deserted kingdom, the ponies are saved from drowning in an underwater cavern by the seapony Princess Skystar, who leads them to her undersea home of Seaquestria. Skystar identifies her kind as the hippogriffs, transformed by a magic pearl used by her mother, Queen Novo, to hide from the Storm King. When Novo denies them the pearl to use against the Storm King, Twilight desperately attempts to steal it while letting her friends unknowingly distract the seaponies. Her plan backfires when she unwittingly triggers an alarm, prompting the outraged queen to banish the entire group to the surface. Twilight argues with her friends over her actions, with the two sides separating after she denounces them for their irresponsible behavior.
Twilight is kidnapped by Tempest, who gains her sympathy after revealing how the loss of her horn caused her own friends to shun her for her dangerously unstable magic as a filly. After Spike alerts the ponies to Twilight's capture, they are joined by Capper, the pirates, and Skystar to help them return to Canterlot and rescue her. Tempest delivers Twilight to the Storm King, who absorbs her and the other princesses' magic into his staff. When Twilight's friends infiltrate the city and defeat the Storm King's guards, he conjures a tornado with the staff, betraying Tempest as well. Twilight saves Tempest and reconciles with her friends, who help her take the staff and end the storm. The Storm King hurls a magical orb at the group to petrify them, but Tempest jumps in his way, turning them both into stone. The Storm King's body falls and shatters, while the group use the staff's magic to revive Tempest, who restores the princesses and the damaged city by returning the stolen magic.
The Friendship Festival resumes, and the ponies celebrate with all of the allies Twilight's group have made on their adventure. Encouraged by Twilight, Tempest joins in by producing a fireworks display with her broken horn, and happily accepts the group's friendship.