The movie begins with Rachel, Cassius, and Vanellope von Schweetz being kidnapped by Doctor Gaster, the movie's main villain, who controls a machine of power called the "CORE". He arranges a wedding between Rachel and Cassius and uses the hypnotic powers of his ally Goner Sloth to force them into marriage. As foretold in the Delta Rune, their marriage summons the Dark Fountain, which Gaster uses to open a black hole known as the "Angel's Heaven" which will eventually grow large enough to destroy the universe. Renee meets Toby, a small dog, who transports her to the Arcade. There, Renee meets Seam, who tells her that she matches the description of the Hero described in the "Under Tale," another prophetical tome. According to the Under Tale, the Hero will travel to various dimensions to collect seven Human Souls, which can banish the Dark Fountain and reverse the destruction. The tome also mentions that the Hero will ally with three other Heroes. Renee and Seam set off to collect the Human Souls and stop Gaster's plan. To stop Renee, Gaster periodically sends out his minions: Goner Brute, a grey warrior; Goner Kid, an immature shapeshifter; and Jevil, a mysterious dimension-traveling jester.
After Vanellope, Cassius, and Rachel escape, they team up with Renee and Toby to find the Human Souls.
A series of flashbacks tell the story of a romantic relationship between two individuals, Wingdings and Tobias, who hail from rival clans. Wingding's disdainful father forcibly ended their relationship and banished Tobias to wander between dimensions and eventually die. It is gradually revealed that Toby is Tobias and Gaster is Wingdings, who, not knowing that Seam transformed Tobias into a Dog, was driven insane by her loss. Wingdings sought to bring existence to ruin and turned to the Delta Rune. Throughout the game, Wingdings and Tobias begin to realize the other's true identities, and Winggings begins to regret his actions, but continues with his plans, knowing that he has gone too far to stop.
After collecting all the Human Souls, the group enters Card Castle and defeat Goner Brute and Goner Kid, but lose contact with Cassius and Vanellope in the process. Renee, Rachel and Tobias confront Jevil, who intends on betraying Wingdings. Jevil also reveals that he anonymously helped the group during their journey, which includes helping Vanellope and Cassius escape. When Renee refuses to ally with Jevil, Rachel fights and defeats Jevil, who seemingly kills himself, bringing Rachel with him. Renee and Tobias continue their journey through Card Castle.
They confront Wingdings but are unable to attack due to the Dark Fountain granting him invincibility. Vanellope, Cassius and Rachel reappear, and use the Human Souls to destroy Gaster's defenses and defeat him, but fail to halt The Angel's Heaven's destruction. Jevil appears and takes control of the Dark Fountain, revealing that he has studied the Delta Rune extensively and wishes to use the Dark Fountain and the Angel's Heaven to create a new universe of pure chaos. Jevil fuses the Dark Fountain, a brainwashed Rachel, and himself into one entity called THE WORLD REVOLVER, who shatters the Human Souls and begins making his new universe. However, Wingdings and Tobias' renewed love and the loyalty of Wingdings' remaining minions restore the Human Souls. Renee defeats THE WORLD REVOLVER and Jevil dies, but leaves behind a fragment of his power to control the Dark Fountain and complete the destruction of all worlds. As such, Wingdings leads everyone to the chapel where Cassius and Rachel were originally married. There, he and Tobias use their renewed love to summon the Human Souls, destroy the Dark Fountain, and seal Angel's Heaven.
Afterward, Renee and his party reawaken in Arendelle. Tobias and Wingdings have vanished; Seam suggests they died when the Dark Fountain was destroyed, but Goner Sloth states her firm belief that the two are still alive. A post-credits photo implies that Tobias and Wingdings have regained their original forms and are alive elsewhere.
While Cassius is locked in the fungeon, his mother looks through the door, holding keys. She tries one key, but the door doesn't open. Queen Harly uses her expired credit card to open the door, and Cassius says he's going to be a good guy.
Rachel wakes up, and she sees that her legs are gone (replaced by a blue tail with lavender fins). A mermaid takes Rachel's nightgown bodice off, the mermaid puts a white seashell bra on Rachel. Rachel says she is a princess. She steals a mermaid's tiara, and Rachel puts it on her own head. Rachel goes to the underwater office.
- “Karla-Lani-Lani-Lani Evil Incorporated!”
- ―Karla Sali
Karla Sali plans to kidnap and kill Rachel.