Yu-Gi-Oh! Zexal focuses on Yuma Tsukumo, a youngster who aspires to become the duelist champion, but usually gets himself in trouble, due to his reckless nature. Something unexpected happens when he challenges Ryoga Kamishiro to a duel. During the duel the mysterious ghost of Astral appears before him and tells Yuma that his mission is to search for his lost memories, that were scattered across the world taking the form of 99 Exceed monsters called "Numbers", and to retrieve them, he must defeat the owners of each Number monster in a duel.But what is Astral's true purpose for appearing here? And what are those new monsters known as "Number Monsters"? A series of mysterious powerful rivals begin to appear before Yuma and Astral, which begins to explain the mystery...
With this combination, the curtain on a new Dueling Legend is about to rise on the world!
Frustrated by his loss against Yuma, Vector dives into the center of his planet, into the Sea of Ill Intent, in order to free the Barian God, Don Thousand. Then, Vector offers his life to Don Thousand, and uses his power to resurrect him. Don Thousand grants Vector his power in exchange for locating the seven Legendary Number cards that sealed him away long ago. To achieve his plans, Don Thousand merges with Vector, and briefly possesses him, while restoring his injured body. Vector uses Don Thousand's powers to revive Mr. Heartland as a fly, who had fallen into Barian World since the events of the previous series, and he manages to locate some of the Legandary Numbers with assistance from Mr. Heartland. Then, Vector uses his new powers to accelerate the healing of Alito and Girag. Meanwhile, Astral brings Yuma, Tori, Shark and Rio aboard the spaceship, informing them of the Numbers scattered across the world. He also shows Yuma a message from Kazuma, saying they will need to obtain the legendary Numbers before Barian World can. As they head to their first location, they end up crashing into Dumon and breaking his Baria Lapis, who ends up in a jungle, injured and stuck in his human form. Yuma doesn't recognize him, and wants to help him out despite Shark's warning to not trust others so easily. They soon come across a temple. After inadvertently activating a trap, Shark and Dumon, who decides to use the alias Nasch (the name of one of the 2 missing Barian Emperors), become separated from Yuma and the others, forced to go down separate paths. Yuma's group ends up in the legendary Number's chamber, where it is protected by its guardian, Mach, who challenges Yuma to see if he is worthy. Making matters worse, the walls in the room Shark and Dumon are trapped is start closing in, requiring Yuma to win quickly in order to save them.
Yuma's attacks help open the way for Shark and Dumon to escape to safety, but come at the risk of receiving damage from Mach's traps and spells. After Yuma summons out Utopia, Mach brings out his own Number, Number 44: Sky Pegasus, which forces Yuma to take more damage to keep Utopia on the field. As Shark and Dumon make their way through each room, they find murals depicting a tragic legend about a white pegasus. Wanting to learn how the legend ends, Dumon urges Yuma to keep protecting Utopia, believing the legend is about protecting your friends. Although Dumon reveals his true form, after Shark's power repairs his Baria Lapis and he recovers his energy, Yuma chooses to protect Utopia. With Astral helping Yuma find a loophole in Mach's combo, Yuma manages to bring out Utopia Ray Victory and win the duel. Mach explains the rest of the legend before leaving Yuma with the Number card, while Dumon states he will settle things with Yuma next time. Yuma also finds a coin which he believes to be a memento from Kazuma.
As Yuma and co head towards the location of the second sealed Number, Vector goes to see Number 96, who has been possessing a corrupt official, and convince him to join up with him in his search for the Numbers. Arriving at an abandoned castle, Vector feels an odd connection to the place, like he had been there before. As Yuma's group arrives, Rio feels a similar sensation, speaking of a legend behind the castle. Vector and Number 96 reach the central colosseum, where Number 96 comes face to face with the Number's guardian. After accidentally triggering some traps, Yuma's group also wind up in the colosseum, where Vector arranges for a duel between Astral and Number 96, who had obtained the sealed Number. Number 96 instantly summons out Dark Mist whilst Astral summons Utopia, managing to use Dark Mist's ability against him. However, Vector reveals that damaging Number 96 activates some of the colosseum's deadly traps, which are aimed right at Yuma.
Number 96 summons out the sealed Number he obtained, Number 65: Djinn Buster, managing to destroy Utopia deal a lot of damage to Astral by taking advantage of his wish not to hurt Yuma. As Astral turns to defensive play, Number 96 uses Barian's Force to evolve Djinn Buster into Chaos Number 65: King Overfiend, with Astral managing to survive by reviving Utopia. Receiving some encouragement from Astral and another one of Kazuma's coins, Yuma manages to use the trap aimed at him to his advantage and move to safety, allowing Astral to fight without hesitation. Astral summons Utopia Ray, but Number 96 uses Barian's Force again to upgrade Dark Mist to Chaos Number 96: Dark Storm, using its abilities to force the match into a draw. Vector then sets the castle to self-destruct as he and Number 96 escape, but Yuma and the others safely escape thanks to Kite's arrival. As Kite is informed of the situation, Girag and Alito awaken from their slumber.
Yuma and the others travel to Spartan City in Rome, where they learn of a duel tournament that Nistro is participating in, with Dextra serving as his manager. Nistro explains to Yuma how he and Dextra, who both grew up on the streets, found hope in Duel Monsters and wanted to give that same hope to children using his new "Star Man" persona. They then tell them about a legend involve a fighter who made friends with a rival, but was ultimately betrayed and executed, stating that the colosseum where the sealed Number lies is somewhere at the bottom of a lake. Later that night, Alito sets off some bombs to drain the lake, revealing the hidden colosseum. Alito enters the colosseum and defeats the sealed Number's guardian, claiming the Number just as Yuma and the others arrive at the colosseum. Alito, who seems to have no recollection of his friendship with Yuma, puts Nistro under his control and challenges Yuma and Dextra to a tag duel. Yuma summons out Utopia whilst Nistro summons Alito's new Number, Number 54: Lion Heart, dealing a large amount of damage to both Yuma and himself.
Dextra manages to protect Yuma after Alito forces Lion Heart's effect to activate again, bring Nistro's life points to 0, but he is revived due to Lion Heart's overlay effect which restores his life points, though this causes damage to his body. Alito then summons out Battlin' Boxer Cheat Commissioner, which once again forces Utopia to fight against Lion Heart, but Dextra manages to redirect the attack to herself. Dextra then summons out her Xyz Monster, Night Butterfly Assassin, and, unable to prevent Alito from forcing her to fight against Lion Heart, puts all her feelings into her attack in the hopes that Nistro would remember his true desire, getting knocked out in the process. Nistro, regaining control of his fighting spirit, forgoes powering Lion Heart up with Barian's Force in order to fight Yuma fairly. Yuma then summons out Heroic Challenger Excalibur in order to fight a heated duel against him. When Alito tries to interfere and force Nistro to use Barian's Force, Yuma counters with a trap that knocks Alito out. When he is defeated, Alito experiences flashes of a past memory, seemedly that of the legendary fighter, while Nistro is freed from Barian control. Nistro then gives Yuma Lion Heart, before returning to the tournament scene to bring hope to children.
While examining the two sealed Numbers they have obtained so far, Astral sees a visions depicting the people in their respective legends as Dumon and Alito. The group soon arrive at the base of a tall rock structure, the top of which lies the fourth sealed Number. As they start climbing the structure, they hear a strange roar that resonates with Kite's Galaxy-Eyes. They arrive at a strange dojo where they meet a man named Jinlon, who guards the sealed dragon Number. As Jinlon mentions that he knows of Mizar, Astral reveals his findings to the other, believing that the Barian Emperors were once human long ago. Kite then challenges Jinlon to a duel with their dragons on the line, with Jinlon summoning his number, Number 46: Dragluon, also summoning out Protector Dragon, which keeps Dragluon from being attacked. When Kite summons Galaxy-Eyes Photon Dragon, its effects are negated by Dragluon, but Kite manages to use other means to destroy Protector Dragon. As Mizar arrives at the bottom of the structure, Jinlon uses Dragluon's ability to summon Drain Dragon, which uses its effect to add Kite's life point value to its attack points, raising its attack points to 8000. Drain Dragon also has an effect that deals half of its ATK points as damage when it is destroyed.
Kite sacrifices some of his own life points, so that he can weaken Drain Dragon and destroy it with Galaxy-Eyes Photon Dragon without losing to Drain Dragon's effects. Jinlon then uses Dragluon's ability to take control of Galaxy-Eyes, but Kite manages to stop its attack and reobtains Galaxy-Eyes so he can summon Neo Galaxy-Eyes Photon Dragon and defeat Jinlon. After the duel, Jinlon tells the others about Mizar's legend, who had formed a bond with Dragluon. When the village wanted to sacrifice Dragluon to ward off rainy weather, Mizar prepared to sacrifice himself to save Dragluon, but they were both struck down by the king's army. Mizar overhears this legend and denies it, preparing to fight against Kite. However, their resonance causes the dojo to collapse, forcing Mizar to retreat. The dojo then disappears, with Jinlon leaving Dragluon in Astral's hands, warning them of a potential disaster that resonates all too well, who feels his mission is to destroy Barian World, but he decided to give the number to Kite, so that he can defeat Mizar and see who is the true Galaxy-Eyes Master.
Yuma returns home and watches a news report about a stone statue of a commander named Kiraku Souhachi from the Warring States period discovered at Roku's Duel Sanctuary. The statue bears a striking resemblance to Girag, and believing there is a Number card to be found, Yuma, Astral, and Tori go check it out. Girag, having returned to the human world, also sees the report and gets to the statue before Yuma and his friends. A Number card pops out of the statue, but then a tanuki spirit emerges from the statue and possesses Girag. When Yuma and company finally arrive, they are surprised to see that the tanuki spirit, Ponta, is in control of Girag's body while Girag himself is in the statue. Ponta is in fact the Number's Guardian, and Yuma challenges him to a duel with the Number card and Girag at stake. After Xyz Summoning Number 64: Ronin Raccoon Sandayu, Ponta temporarily possesses Yuma and proceeds to waste all of Yuma's cards in a series of misplays. Nonetheless, Yuma manages to win the duel and claim the Number. It is revealed that in the legend of Girag, Ponta was just a stray animal picked up by Girag and had the ability to transform himself into a duplicate of Girag, allowing Ponta to act as his double for battles. However, Ponta was betrayed by Girag, who sent him away before a big battle, making Ponta angry, and his spirit had been sealed in the statue ever since then. Girag defends himself by saying that he drove Ponta away because he knew he was entering a losing battle, and he wanted Ponta to stay alive. Girag, in spirit form, then bursts out of the statue and swallows Ponta, reclaiming his body. He then departs back to Barian World, with Ponta's spirit resting inside him.
As the gang arrive at the location of the final two sealed Numbers, above a stormy ocean, Rio suddenly starts hearing a voice in her head and is drawn towards the ocean; and she dives into it. Shark, Yuma and Astral dive in after her and wind up in a mysterious world underneath the sea, following Rio's footprints to a strange labyrinth, where Shark becomes separated from the others. Arriving at a temple in the center of the labyrinth, Shark finds Rio, who has been possessed by the Number's guardian, Abyss, and is challenged to a duel. Sharks summons out Black Ray Lancer while Abyss summons out Gorgonic Guardian, using its powers to destroy Black Ray Lancer. When Abyss projects a strange light, Shark sees a vision in which he and Rio were rulers of an ancient civilization, which was attacked by Vector. As Shark's life points are knocked down to 200, Dumon appears before Yuma and Astral.
Dumon states his desire to find the two missing Barian Emperors, Nash and Marin, while Astral responds that his mission is to destroy the Barian World. Meanwhile, Shark encounters more visions while Abyss summons his namesake, Number 73: Abyss Splash. Astral and Dumon are brought into one of Shark's visions, in which Rio sacrificed herself to help Shark fight off Vector, leading to the realization that both Shark and Rio are the missing, former Barian Emperors. As Abyss attempts to sacrifice Rio in the same manner, Yuma manages to save her whilst Shark becomes able to summon Rio's Number card, Number 94: Crystal Zero, and win the duel. As Shark receives Abyss' card, everyone returns to the ship, but Rio remains unconscious.
As various supernatural disasters happen across the world, Number 96 appears and brings Yuma, Astral, Tori, Shark, and Kite to a Chaos Field, forcing Yuma and Astral into a Sphere Field that barrages them with lightning. As the duel goes on, Number 96 manages to summon Chaos Number 96: Dark Storm, before using the field spell Chaos Field to steal Yuma's Number 69: Heraldry Crest and Number 92: Heart-eartH Dragon, and rank them up into Chaos Number 69: Heraldry Crest of Horror and Chaos Number 92: Heart-eartH Chaos Dragon. Number 96 then uses the ability of Heart-eartH Chaos Dragon, which prevents Yuma from activating card effects of cards on the field until the End Phase, making Yuma unable to avoid Number 96's attacks.
After barely managing to survive Number 96's attack, with the ability of Bacon Saver, Astral helps Yuma with his duel. Using the special ability of Heart-eartH Chaos Dragon, Dark Mist raises his Life Points to 7,500, while Yuma only has 500 Life Points remaining. Being unwilling to give up, Yuma and Astral merge into ZEXAL II, and bring out Utopia Ray and two new Zexal Weapons: Sleipnir Mail and Asura Blow. This allows Yuma to overpower Number 96's monsters and defeat him. In a last-ditch attempt, Number 96 uses the last of his strength to try and take over Astral's body, but Astral chooses to sacrifice himself to destroy Dark Mist, leaving Yuma horrified. This action severely drains Astral and forces him to retreat to Astral World, and he entrusts Yuma with the Numbers they obtained, before fading away.
As Yuma remains reclused following Astral's disappearance, Don Thousand gives Vector the remnants of Number 96's power, who is revealed to be a shard of Don Thousand's malice that was trapped inside of Astral, during Astral's ancient battle with Don Thousand. Number 96 is also revealed to be a "Forbidden Number." Then, Don Thousand reveals his plan to use his new powers from Number 96 to make multiple Dimension Fusing Devices, to merge the Human World with Barian World, once the level of evil in the Human World reaches that of Barian World. This would increase Don Thousand's power by a thousandfold, giving him enough power to destroy Astral World. In order to create more Dimension Fusing Devices, Don Thousand emerges from Vector's body in a black energy form resembling his true likeness, and fuses Vector to his throne, in order to concentrate their energy on making more Dimension-Fusing Devices. Then, using his newly enhanced powers, Vector returns Mr. Heartland to his human form, grants him four Fake Number cards, and gives him a group of 3 Barian servants, who, along with Mr. Heartland, make up the Fearsome Four of the Dark Dueling World. Mr. Heartland distributes 3 of the Number cards among the other members of the Fearsome Four, while he keeps Number 1. Soon afterwards, a servant named Semimaru begins attacking duelists and stealing their memories. When Tori and the others try looking into the incident to cheer Yuma up, they are caught by Semimaru, who steals their memories and uses them as bait to lure Yuma into a duel. Heartland attempts to coerce Yuma into giving up his Numbers to save his friends, but he remains determined to cling onto the Numbers that Astral had left him. He is soon joined by Trey, who offers to support Yuma in a 2-on-1 duel against Semimaru. However, Mr. Heartland uses Don Thousand's power (which manifests in a crest-like form of Don Thousand's Barian Emblem) to activate a field effect, which puts Yuma and Trey at a distinct disadvantage
Semimaru quickly summons out the Number he received from Vector, Number 3: Cicada King, using its ability to negate a combo Yuma had planned to use with Utopia. Trey summons Number 33: Chronomaly Machu Mech, managing to damage Semimaru with help from Yuma's cards. However, Semimaru deals a lot of damage to Trey, who took the hit for Yuma, and activates a trap that would ensure Yuma's victory on his next turn. As Yuma struggles to think of a comeback, Tori and the others regain some of their memories and show their support, reminding Yuma that he is not alone. Yuma then sets the stage for Trey to summon Number 6: Chronomaly Atlandis, equip it with Utopia, and use Atlandis to win the duel, destroying Semimaru and returning Tori and the others to normal. Afterwards, Yuma decides to give Cicada King to Trey as a sign of their friendship.
Chironex uses Number 4: Stealth Kragen's ability to summon two Kragen Spawns, bringing back Stealth Kragen and another Spawn when Quattro uses Giant Grinder's ability again. As the poison continues to worsen Shark's condition, Quattro summons Number 40: Gimmick Puppet of Strings, but it has its abilities blocked by Chironex's trap card. After receiving encouragement from Quattro to stand up, Shark manages to summon Abyss Splash and works together with Quattro to defeat Chironex. This allows Shark and Rio to be cured of the poison, and earns Quattro the Stealth Kragen card. Before disappearing, Chironex remembers that he was responsible for the car accident that killed Shark's family. However, he muses that Shark and Rio shouldn't be here, because he remembered that they were killed in the accident. Afterwards, Shark finds an emblem in his family's mansion, similar to the one he saw in his visions of his past life (the Barian Emblem), implying that he and Rio had died in that accident.
As Yuma continues to put on a brave face around the subject of Astral, Flip builds a memorial for him to show everyone's respects. However, Yuma still refuses to acknowledge Astral's death, even when the others try to confront him about it. Just then, Kite appears before him, stating that they may find a way to bring Astral back, if they can find a way into Astral World to search for the Numeron Code. He states that they could use the coins left by Kazuma, which are believed to be fragments of Astrite crystals, to power an interdimentional gate to Astral World. He takes Yuma and Tori to the location of an interdimensional gate he and Quinton built, where they manage to convince Quinton to let him go, despite the dangers involved. As the preparations are made to send Yuma to Astral World, Heartland's third minion, Scritch, attempts to interrupt the experiment, challenging Kite and Quinton to a handicap duel. Quinton and Kite summon Number 9: Dyson Sphere and Galaxy-Eyes Photon Dragon respectively, while Scritch summons his monster, Number 2: Ninja Shadow Mosquito, which is hidden from sight.
After Kite and Quinton discover that Ninja Shadow Mosquito is literally as small as a mosquito, Scritch uses its ability to make Galaxy-Eyes Photon Dragon attack Quinton. Meanwhile, Kite is affected by a mosquito bite he received from Scritch during his journey, which is causing him to confuse his allies with his enemies. Recalling his training days with him, Quinton manages to awaken Kite's inner fire and break him free of the Scritch's influence. With help from Quinton, Kite manages to power up Galaxy-Eyes Photon Dragon and defeat Scritch, and obtain his Number card. After the duel, the interdimensional gate is fully charged, allowing Yuma to go to Astral World.
Arriving in Astral World, Yuma is guided by a Rainbow Kuriboh Kazuma built towards a strange town, where he is attacked by a strange being named Eliphas. Escaping thanks to Rainbow Kuriboh, Yuma receives a message from Kazuma, telling him to save Astral. Meanwhile, Shark, who is conflicted between his childhood memories and Barian memories, is approached by Dumon, who reveals to Shark that he is one of the Seven Barian Emperors, Nash. Yuma is rescued by an Astral being named Ena, who states Yuma can use the power of Chaos to restore the damage done to Astral World, and help its people fight against Eliphas, who has put the town under his control. With Ena's help, Yuma finds where Astral is laying, with Eliphas standing in his way. As the two begin to duel, Eliphas summons his Xyz monster, New Order 4: Etheric Anubis, while Yuma summons Utopia. However, Yuma is soon pushed into a corner when Eliphas exhibits the ability to perform a Shining Draw.