Delinquent racer Jungle Pocket, Yuri Fujimoto, travels to the racetrack with her friends, where she witnesses Fuji Kiseki, Eriko Matsui, win a race and glow with new purpose. Inspired by that standout performance, Jungle Pocket decides to become a Twinkle Series racer herself and enrolls at Tracen Academy to join Fuji Kiseki's team led by Kenichi Ogata Tanabe. With grit and a growing sense of belonging, Jungle Pocket clinches wins in her preliminary races, paving her path toward her first high-profile test at the Hopeful Stakes.
On the way in, Jungle Pocket meets the eccentric Agnes Tachyon, Sumire Uesaka, and her confidence begins to tilt at the edges. Jungle Pocket remains certain she can prevail in the Hopeful Stakes, only to be toppled by Agnes Tachyon in a sharp upset, shaking her resolve and foreshadowing a fierce rivalry. Between that setback and the sight of the undefeated T.M. Opera O, Sora Tokui, sweeping the Arima Kinen, Jungle Pocket finds a renewed hunger to push past her limits and to defeat them all.
Determined to close the gap, Jungle Pocket directly challenges Agnes Tachyon and declares her as a rival, a moment that also introduces her to Dantsu Flame, Haruna Fukushima, and Manhattan Cafe, Yui Ogura. Agnes Tachyon accepts with a sly calm and begins to shadow Jungle Pocket’s training and races, even as she wins another race against Manhattan Cafe. Amid the growing battles on the track, Fuji Kiseki opens up about an impending retirement before the Japanese Derby due to a leg injury, and she shares a hopeful wish: Jungle Pocket could win the Derby and fulfill her promise to make Tanabe a true Derby Trainer, a dream that binds their fates.
The rivalry heats up as Jungle Pocket and Agnes Tachyon meet again in a rematch at the Satsuki Shō, this time with Dantsu Flame by their side, though Jungle Pocket is again bested. Agnes Tachyon later announces an indefinite hiatus from the Twinkle Series, leaving Jungle Pocket furious and puzzled by her rival’s sudden departure. The young racer confronts Agnes Tachyon about abandoning their duel, only to hear that Tachyon’s heart now leans more toward research than racing. As Jungle Pocket departs with Dantsu Flame and Manhattan Cafe, Agnes Tachyon cryptically muses that she would like to see them rise above her.
Tanabe sits down with a frustrated Jungle Pocket and suggests that Agnes Tachyon’s drive to surpass every limit may have taken a toll on her leg, urging Jungle Pocket to keep training. The two later duel again in the Japanese Derby, with Agnes Tachyon watching closely, hoping her provocations will spur Jungle Pocket to push beyond what she thought possible. Jungle Pocket finally wins and, alongside Fuji Kiseki and Tanabe, fulfills a long-held promise, while Agnes Tachyon comes to accept that her rivals’ victories keep moving forward without her and retreats into reclusion.
Even with that triumph, Jungle Pocket battles lingering self-doubt about proving herself against Agnes Tachyon, and she stumbles in the Kikuka-shō against Manhattan Cafe. Seeing her pupil struggle, Fuji Kiseki challenges Jungle Pocket to a duel that rekindles her initial spark and purpose. Jungle Pocket then visits a lonely Agnes Tachyon, reaffirming her desire to face her rival again despite the doubt, before heading to train for the Japan Cup.
At the Japan Cup, a resolute Jungle Pocket faces off against T.M. Opera O, and she overcomes her doubts in the critical final stretch to claim victory. Agnes Tachyon, moved by Jungle Pocket’s relentless drive, decides to end her hiatus and watches as her rival rises to the top. A future race then offers a fresh rematch opportunity between Jungle Pocket and Agnes Tachyon, joined by Dantsu Flame and Manhattan Cafe, and the four share a triumphant culmination in a Winning Live Concert that seals their rivalry, friendship, and a shared love of racing.