After school, Ichika Usami, Karen Miyama, gathers with friends for a light picnic on a hill near a tree stump and recounts a vivid dream: a girl and her fox friend Shizuku Yoshino Kimura are fleeing from Akainu and Kiinu. In the dream, Shizuku hands Sakura Kana Asumi three cards and tells her to look for the symbols on them to find help, then pushes Sakura through a portal, separating them as Shizuku arrives in Ichigozaka.
Ichika then meets the girl from her dream, Sakura Kana Asumi, who notices a pastry depicted on one of the cards and even tries to grab Ichika’s cupcake. Before Ichika can ask about the cards’ meaning, Akainu attacks. Ichika transforms into Cure Whip to fight, and Sakura realizes that the cards’ purpose is to guide them to the Pretty Cure whose symbol matches each card. As Sakura struggles to defend herself, she wishes she could help, and her Miracle Light, the Miracle Sakulight, glows and opens a door that she walks through, where she briefly explains the Miracle Lights to the audience. After the other Kirakira Cures arrive and help Whip defeat Akainu and revert it to origami, Sakura explains what happened and they theorize that what’s happening to Sakuragahara is affecting the cherry blossoms in their world.
As the Cures search for the Cures of Keys and Jewels, Ichika, Himari Haruka Fukuhara and Aoi Tomo Muranaka travel to the Magical World, where they investigate Mofurun Ayaka Saito because her jewel matches the symbol on a card. In the shopping district, Akainu sends a Yokubaru to attack them, and the Mahou Girls Cures come to their aid. Meanwhile, Yukari Kotozume, Saki Fujita, and Akira Kenjo, Nanako Mori, go to Noble Academy, where Akira intimidates Yui Nanase, prompting the Princess Pretty Cures to confront her; the two teams then join forces to fight a Zetsuborg sent by Kiinu. A mysterious girl named Samidare appears and later attacks Sakura, but retreats when she hesitates to harm her.
At the KiraKira Patisserie, the Cures and Sakura share dessert, and Sakura is melancholy as she remembers her promise with Shizuku to see the cherry blossoms bloom. The Miracle Sakulight glows again and forms a door at the tree stump, which Sakura opens to lead the Cures into Sakuragahara.
Once there, Akainu and Kiinu fuse into Ooinu, and Karasu Tengu confronts the group, telling Sakura they want to use her portal-opening ability to travel to other worlds. The Cures struggle to stop them as Samidare reappears and turns the Cures into origami, sparing Whip and Sakura. Whip fights Samidare, shattering half of her mask and revealing an eye that Sakura recognizes as Shizuku’s, leaving her shocked that Shizuku has turned evil. Whip remains determined to save Shizuku, while Sakura grieves that Shizuku no longer remembers her. Yet Whip’s vow to protect her family and friends causes the Miracle Sakulight to glow and restore Sakuragahara to its normal state. Sakura tries to reach Samidare’s true form, helping her remember as the mask shatters completely and Shizuku is returned to normal along with the other Cures.
As the Cures battle Karasu Tengu, who powers up, they urge the audience to support them with the Miracle Lights. Sakura recalls how she used to be afraid but has grown braver since meeting the Cures, and with the Miracle Sakulight she opens the door to Sakuragahara. The Cures, together with Sakura and Shizuku, guide a giant form of Whip made of Kirakiraru and, with Sakura and Shizuku’s help, strike at Karasu Tengu’s weak spot—the nose—and defeat him. The film closes with a flower-viewing moment, where Whip thanks Sakura for helping realize her dream of sharing the cherry blossoms with friends.