Months after the conclusion of the VF Circuit, Aichi enters high school as a freshman at Miyaji Academy. However, he has trouble adjusting to his new school life due to the academy's heavy emphasis on studies. After school, Aichi goes to Card Capital while being tailed by a classmate, Naoki Ishida. There, he sees the many customers playing Vanguard, which Naoki has no knowledge about. He spots Aichi conversing with Team SIT Genius in the back of the shop. Curious by how different Aichi's behavior is in the card shop compared to how he acts at school because of a card game, Naoki becomes intrigued to Vanguard. And so, Aichi teaches Naoki about Vanguard through playing an actual match, with the latter being lent a new Narukami trial deck to use from Shin. As they cardfight, Naoki slowly gets immersed into the game. After Aichi eventually wins, Naoki buys the trial deck and hastily leaves in a frustrated manner, which worries Aichi.

The news of Kourin transferring into Aichi's class becomes a hot topic, especially when the male classmates start talking to Aichi to get closer to her once they learn that the two know each other. Then, Aichi gets an idea on how to promote Vanguard at his school. Because there is no Cardfight Club, Aichi decides to make one himself. The next day, he tries to recruit enough members to officially start the club (needing a minimum of five people, including himself) by handing out leaflets in front of the school. His pleas fall on deaf ears until Kourin agrees to be a member. Her enlistment is followed by several other boys who want to join (only to be with Kourin), but she proposes that anybody who wants to become club members will have to defeat either her and Aichi in cardfights before they can enter. The two easily beat all of the challengers, but then Naoki steps up to play against Kourin with honest feelings of wanting to join the club.

Aichi's Cardfight Club is attracting attention all around the school as male classmates (who are mostly interested in being with Kourin) have him teach them the rules of Vanguard and again attempt to play against Kourin in order to be inducted to the club but to no avail. Additionally, the female students gossip about a rumor that claims Aichi only started the club to get close to Kourin, which makes Misaki worry. Aichi tries to ask Misaki to join the club, but she declines because of her job at Card Capital. Kourin gets an unsettling feeling that there is someone watching her, with Naoki suspecting that it could be a stalker. Naoki eventually confronts the stalker who turns out to be a classmate, Shingo Komoi. Naoki threatens to beat him up, but Shingo suggests to settle things with a cardfight instead. Despite modifying his Narukami deck, Naoki's inexperience at Vanguard causes him to struggle against Shingo's Murakumo deck.

The student council president of the Miyaji Academy High School Division deems Aichi's Cardfight Club to be unnecessary for the school and orders the vice president, Suwabe, to devise on how to abolish it. Elsewhere, the Cardfight Club finds an empty classroom to serve its official headquarters. Then, the school's American football team, the Miyaji Vipers, barges in and takes the club outside to the academy's sub-ground where the Vipers' quarterback/captain, Ikki "the Catapult" Kongou, challenges Aichi to a cardfight, with the former appropriately using a Spike Brothers deck. This is an elaborate plan set up by Suwabe to have Ikki defeat Aichi and thereby crush the Cardfight Club members' spirits into not wanting to continue the club. Ikki uses strong Limit Break effects of the latest Spike Brothers to push for victory, but Aichi successfully defends and makes it to his next turn.

After Aichi tells his friends at Card Capital about how his school's student council is causing problems for the Cardfight Club, he repeatedly requests for Misaki to join as the fifth member. However, she still turns him down, having mixed feelings on the matter and being insulted by Kourin for not being serious on becoming a member. Then, to quickly shut down of the Cardfight Club, the student council creates a deadline for all potential clubs with at least five members to report to the council, or else they will not be officially recognized by the school. At the last second, Misaki declares herself as the Cardfight Club's fifth member after resolving her feelings of earnestly wanting to join the club. As an initiation test and to prove herself to Kourin, Misaki cardfights Aichi.

Miyaji Academy's unofficial Cardfight Club is set up to have an intramural match against Hitsue High School's Vanguard Club, in which Kai, Miwa, Morikawa, and Izaki are members. The two teams play in a best-of-5 match, and opponents are randomly selected. Under the conditions that the Miyaji Academy student council president created, if the Cardfight Club loses this match, then it will be dissolved. In the first game, Naoki fights Kai, with both using Eradicator-themed Narukami decks. Naoki combines both the Break Ride of Eradicator, Vowing Sword Dragon and the Limit Break of Eradicator, Gauntlet Buster Dragon to retire Kai's units and gain more critical value and power, but Kai manages to survive the assault. Then, Kai uses a similar devastating combo with Vowing Sword and Eradicator, Dragonic Descendant. Although Naoki blocks his first attempt, Kai activates Descendant's Limit Break to have it stand up, gain another critical, and attack again.

Kourin defeats Izaki, which ties the score 1-1. The third game pits Misaki against Hitsue Vanguard Club's ringer and old Q4 teammate, Kamui Katsuragi. Although Kamui gets an early lead, Misaki mounts a comeback with Battle Deity of the Night, Artemis. Kamui then combines the Break Ride of Beast Deity, Ethics Buster and the Limit Break of Ultra Beast Deity, Illuminal Dragon to stand four of his rear-guards to launch multiple attacks in one turn. However, Misaki protects herself, only taking one point of damage from Kamui's five attacks. In what seems to be a hopeless situation, Misaki rides Eternal Goddess, Iwanagahime and uses its Limit Break to retire Kamui's front-row units. Weakening Kamui's defenses, Misaki wins and puts Miyaji Academy up 2-1. In the fourth game, Shingo is selected to fight against Miwa. Before the fight, Shingo underestimates Miwa, which ends up being his undoing when Miwa demolishes him and evens the score 2-2. So, it's Aichi vs.

Aichi faces Morikawa in the last fight of this intramural match. Although initially mad with using Kai's Kagero deck and not his own, Morikawa nonetheless puts a great amount of pressure on Aichi. All the while, Kai watches the fight as an opportunity to see if his Kagero deck is strong enough against the current Aichi, who strikes back with the Break Ride of Solitary Liberator, Gancelot to empower itself and his rear-guards. Morikawa defends and makes it to his next turn, in which he rides Dragonic Overlord the End. Pairing its Personablast with the Break Ride effect of Dauntless Drive Dragon, Morikawa attacks Aichi with the End three times in a row. Determined to win for the sake of the Cardfight Club, Aichi withstands the onslaught and then uses Gancelot's Break Ride again on the following turn to land a final blow. Aichi emerges victorious over Morikawa, meaning that the Miyaji Academy Cardfight Club wins the intramural match.

Now that the Cardfight Club has become official, the new faculty advisor Nakamurabashi makes the club decide on a captain and vice-captain for the club by order of the student council president. Since Aichi was the person who started the club, he reluctantly accepts the position of captain. As for who should be the vice-captain, Shingo is the only person who honestly wants the job while the others are apathetic on the matter. Not wanting to make a hasty decision, Nakamurabashi recommends to hold off until tomorrow on who to elect for vice-captain. After school, Misaki is convinced by her friend Akari to try out for vice-captain. The same happens with Kourin being persuaded by Takuto. The club meets the next day, and when Nakamurabashi asks again for who wants to be the vice-captain, Shingo, Naoki, Misaki, and Kourin all raise their hands. To finally settle things, the four cardfight each other with the overall winner becoming the vice-captain.

Shingo tells Naoki about a Cardfight Circle formed in the middle school division of Miyaji Academy. Shingo suggests that the two of them should pay a visit to the circle and build a relationship between it and the Cardfight Club. Naoki agrees, but he is unaware of Shingo's scheme; he plans to use this as his chance to impress the underclassmen and take them under his wing, thereby raising his status over Naoki. The two go to the Cardfight Circle's clubroom where they meet Emi and Mai, who are two of the three members of the circle. Naoki and Mai play a friendly match, in which Naoki shockingly loses to Mai's Bermuda Triangle deck. After the game, he asks her for advice in a somewhat intimidating fashion. But this earns him to be reprimanded by Misaki, who later enters with Aichi. Not knowing that Aichi and Emi are siblings, Shingo gets offended when he hears Emi talking to Aichi in a casual manner, which causes her to get mad with Shingo.

Rekka, the third member of Miyaji middle school's Cardfight Circle, enters the clubroom and is followed by Kourin. After Shingo informs Naoki on who Rekka is, she then challenges Aichi to a Vanguard fight. As the two battle, Rekka shows off her charm as an idol, which infatuates Shingo into becoming her fan. Rekka uses the various effects of her Celestial-themed Angel Feather deck to move cards in and out of her damage zone to her advantage. She gets a copy of Solidify Celestial, Zerachiel into her damage zone which, via the Limit Break of her vanguard Zerachiel, empowers all of her Celestial Angel Feather units. However, Aichi withstands Rekka's assault and uses his Gancelot/Alfred Limit Break Ride combo while also superior calling Blaster Blade Liberator from the soul to finish the game and defeat her. Afterwards, the two clubs give their thanks to each other before Shingo offers to become a member of Rekka's fan club.

The Cardfight Club receives an invitation to and then registers for the upcoming Vanguard Fight High School Championship, a tournament that will feature high school Vanguard teams from all over Japan. Naoki suggests to check out some of the competition, which leads to the club visiting Fukuhara High, an elite private high school that is associated with Team Asteroid. The club is greeted by Tetsu Shinjou, who leads everyone into the school where they watch a cardfight between Asaka Narumi and Leon Soryu, much to Aichi's surprise. Asaka tries to end the game by using Starlight Melody Tamer, Farah's Personablast and the Pale Moon strategy of superior calling units from the soul during the battle phase for additional attacks. Despite the multi-pronged assault, Leon defends himself and then rides Last Card, Revonn on top of Blue Flight Dragon, Trans-core Dragon. This activates the latter's Break Ride effect, forcing Asaka to discard a card from her hand.

After Naoki makes another offhand comment towards Suiko, the two start their cardfight. Suiko criticizes Naoki for being a good but uninteresting fighter. He tries to prove her wrong when he activates the Limit Break of his new ace card: Armor Break Dragon. At the cost of discarding three cards from his hand, Naoki not only eliminates Suiko's front-row rear-guard units, but he also increases Armor Break Dragon's power and critical value to unbelievable heights. Despite this, Suiko defends against Naoki's attacks with almost all of the cards in her hand. On the following turn, Suiko wins the game with Chief Nurse, Shamsiel by moving cards to and from her damage zone thus increasing most of her units' power. Afterwards, Naoki apologizes to his friends for his loss and realizes how weak he actually is. Shingo cheers him up (although with some harsh choice of words) and says that he'll train Naoki to become stronger.

The Cardfight Club is forced by the Miyaji student council to take the main stage on the day of the academy's upcoming School Festival. The student council hopes to use this chance to embarass the club and tarnish its reputation. Despite the daunting task, the club decides to do a stage play using one of Shingo's prewritten scripts and with costume help from Emi and Mai. The script is loosely based on The Tale of the Bamboo Cutter but with Vanguard units; Aichi is given the role of the bamboo cutter (Little Sage, Marron), Misaki is the heroine (CEO Amaterasu), Naoki is the villain (Eradicator, Vowing Sword Dragon), and Kourin is the hero (King of Knights, Alfred). Although Kourin is seemingly busy with her job as an idol, Misaki notices that she is in fact preparing for the play. However, on the day of rehearsal, Kourin does not show up, which leads the club (except Misaki) to think that she is not serious about the play and that Aichi should take the role of Alfred.

The sudden appearance of Daigo surprises everyone and also attracts more students to watch the Cardfight Club's play unfold. Posing as the "real" villain of the play, Daigo is challenged by the hero Kourin to a cardfight for Misaki's freedom. Although Kourin applies a lot of pressure to him shortly into the fight, Daigo eventually gets a heal trigger and deals 5 damage to her, putting her in a tough situation. However, she is cheered on by Misaki and subsequently the audience to not give up. Kourin regains her composure and tries to end the game with the Limit Break of Leading Jewel Knight, Salome. Unfortunately, she does not do so. Daigo then uses White Dragon Knight, Pendragon's Limit Break to superior ride his new ace: Sanctuary Guard Dragon. He activates its Limit Break to overpower and defeat Kourin. Although the hero Kourin loses, Misaki, Aichi, Naoki, and Shingo all step up to challenge Daigo for their fallen friend.

The Vanguard Fight High School Championship finally begins with the Miyaji Cardfight Club having to attend the Kanto regional qualifiers. In the waiting room, the club sees Fukuhara's and Hitsue's Vanguard teams. In particular, Hitsue's team has a surprisingly strong look of determination to win the entire tournament. The first round pits Miyaji Academy against Hitsue High in a best-of-3 match. In the first game, Kai defeats Shingo, which puts Hitsue up 1-0. The second game features Miwa vs. Misaki. For the sake of his teammates, the typically-carefree Miwa goes all out with the Limit Break of Hellfire Seal Dragon, Blockade Inferno to retire all of Misaki's grade 2 rear-guards and gain a significant amount of power. Misaki completely defends herself, but she is left with a weakened battle formation. Nonetheless, on her next turn, Misaki rides Goddess of Good Luck, Fortuna and reassembles her forces.

The decisive fight between Aichi and Izaki ensues. Although Izaki is underestimated by the majority of the people watching, he nonetheless is serious about wanting to catch up to Aichi's level of strength. Aichi notices his fighting spirit and the two continue to play to the best of their abilities. Despite the large amount of pressure from Izaki's Ancient Dragon units, Aichi pulls off a comeback victory. Izaki sheds tears of frustration over this loss, but his effort is rewarded with applause from the crowd. The regional qualifier progresses to the final round, in which the Miyaji Cardfight Club will face off against the Vanguard Club of Fukuhara High.

The members of the Miyaji Cardfight Club draw lots to decide who will play against the Fukuhara Vanguard Club in the final round of the Kanto regional qualifier. Naoki is selected to be first, Kourin is second, and Aichi is third. After some pre-fight conversations between Miyaji and Fukuhara, the two teams send their fighters for the first game. Naoki once again fights against Suiko. Unlike what happened in their previous encounter, Naoki chooses to not preemptively use the Limit Break of Armor Break Dragon in order to maintain the cards in his hand. He survives Suiko's Break Ride combo attack, but he is left in a tough situation and begins to question himself. With some encouragement from Aichi, Naoki trusts his instincts and activates Armor Break Dragon's Limit Break, climactically winning the game and putting Miyaji up 1-0. For the second game, Miyaji's Kourin will face Fukuhara's Asaka.

Kourin and Asaka fight each other in the second game of the final round with both of them having their own reasons to win. Kourin hopes to win for the sake of her teammates while Asaka fights for Ren. The cardfight is a seesaw battle until Kourin deals 5 damage to Asaka. However, this allows Asaka to use a Limit Break Ride combination move with Miracle Pop, Ava and Nightmare Doll, Chelsea. She superior calls more of her units to the field to launch multiple attacks, which gives her the win over Kourin. Although frustrated by this loss, Kourin is comforted by her teammates that they will win in the end. The last fight is coincidentally a rematch between Aichi and Ren, who reverts back to his Shadow Paladin deck but themed around the Revenger archetype.

Aichi and Ren face off in the third and last game of the Kanto regional qualifier. As the fight unfolds, Kai watches and is concerned about them. Despite Aichi's best efforts to land a final attack with Blaster Blade Liberator, Ren survives and finishes the battle with a final blow from his reborn avatar: Blaster Dark Revenger. With that, Fukuhara High wins the regional tournament and therefore moves on to the VF High School Championship. Aichi apologizes to his teammates, but they are not upset by his loss and instead cheer him up. During the awards ceremony, Kai leaves after coming to the conclusion that both Aichi and Ren have become too strong for him. As the Kanto regional qualifier comes to a close, the Miyaji Cardfight Club looks forward to more cardfighting in the future. However, unbeknownst to the club, the Miyaji student council continues to scheme for the club's abolishment...

After reporting to the student council president about the Cardfight Club's loss at the Kanto regional tournament, Suwabe moves on to his next plan of terminating the club. He gets the Paranormal Power Research Society, a group of delinquent-looking students who are interested in supernatural forces, to challenge the club to a cardfight on the rooftop of the school. However, instead of the Cardfight Club, Leon and Team Dreadnought appear and accept the challenge. Nonetheless, Eru Nakagami, the leader of the Research Society, engages in a Vanguard fight with Leon. Nakagami uses his Dark Irregulars deck and also unleashes his sealed paranormal powers to push for victory. Regardless, Leon defeats Nakagami by putting him in a no-win situation with Last Card, Revonn. All the while, the Cardfight Club enjoys lunch along with Takuto.

Aichi has an ominous nightmare in which Misaki, Kourin, Naoki, and Shingo all leave him. Worried about the dream, he then goes to school and is relieved to see his friends are there, except for Kourin. After school, Aichi arranges for the Cardfight Club to meet at Card Capital. Naoki goes back into the classroom to retrieve his bag and then decides to follow the student council's secretary. He is eventually led into a strange hidden room where he sees the secretary talking with an unknown person about monitoring the Cardfight Club. At Card Capital, Aichi expresses his worry to his friends over Kourin's absence. Naoki enters the shop, but he is acting like a completely different person. As if possessed by a dark force, Naoki challenges Aichi to a cardfight, which he accepts. The fight reaches a turning point when Naoki declares "Final Turn" and does a Crossbreak Ride with Eradicator, Vowing Saber Dragon "Reverse".

Kai meets with Takuto and tells him about the incident with Naoki. Takuto explains that it is the work of Reverse, a phenomenon created by the evil Void in its quest to envelop everything in darkness. He further elucidates that those who are Reversed will lose their souls and become engulfed with Void's energy if they lose to a Reversed fighter. It is then revealed that Takuto has been Reversed and is now an agent for Void. The two engage in a cardfight, and Kai is surprised to see Takuto's deck representing Link Joker, a never-before-seen clan that acts as the harbinger of Void. As the fight progresses, Kai is shocked by the terrifying Lock effect of Link Joker; his units are sealed away from being used until the end of his turn.

The fight between Toshiki Kai and Takuto Tatsunagi continues. Takuto repeatedly taunts Kai and tries to tempt him with the power of Link Joker. Kai manages to work around his units being locked, but Takuto is able to defend against Kai's attacks. Ultimately, Takuto succeeds in brainwashing Kai using Reverse. Kai appears unexpectedly at Fukuhara High School.

Possessed by the power of Link Joker, Kai goes to fight Tetsu, a person he deems worthy of passing it on.