Having ended his conflict with Yubel, Jaden returns to Duel Academy in order to complete his third and final year there. Duel Disks cease to function properly, and a new enemy appears.

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Jaden contemplates leaving Duel Academy, as his friends investigate who burned the room of "defective" cards. Jaden again Duels the black-clad man, who calls himself Trueman. Elsewhere, Atticus appears to be having nightmares, and Yusuke Fujiwara continues his mysterious activity.

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Atticus endeavors to recover his lost memories of what happened in the Abandoned Dorm, and Duels Jaden at that location with Nightshroud's "Red-Eyes Darkness Dragon" in the hopes of it acting as a trigger for his memories. Yusuke Fujiwara continues his mysterious activities.

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Yusuke Fujiwara is revealed to be the Duel Spirit of Honest, who was previously the real Fujiwara's Spirit Partner. He vows to avenge his master, but is ultimately talked down by Jaden. Trueman attacks again and Jaden uses Honest's powers to aid in his Duel against him.

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The junior students at Duel Academy organize a Tag Dueling tournament, where the senior students Duel against the junior students.

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The Tag Dueling tournament reaches its final match: Jaden and Alexis against Hassleberry and Blair. Jaden and Alexis still are not working well together, and Blair activates a card allowing them to switch partners. Alexis struggles with her decision on what to do when after graduating and with her feelings for Jaden, which the latter seems oblivious to.

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Zane washes up on the beach around Duel Academy, somehow still alive. A Jinzo Art Duelist named Makoto Inotsume defeats Chancellor Sheppard and wishes to Duel Zane to destroy the Cyber Art once and for all. Zane is still recovering from his heart problems, but Duels Inotsume anyway.

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Syrus takes up his brother's Deck to save the Cyber Art from the Jinzo Art Duelist Makoto Inotsume. While training, he cannot get the Deck to function properly for him, but discovers something about Zane's heart condition in the process.

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Chazz aims to become a Pro League Duelist, but cannot acquire a sponsor. Dr. Crowler arranges for him to become the assistant of Aster in an effort to help him become a better Duelist and learn the basics of the Pro League.

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Chazz Duels Aster in a faux Duel organized by Mike, the duplicitous television producer. Chazz enlists Jaden's help to even the odds, as if he wishes to defeat Aster, then he wants to do it on his own, not due to Mike's interference.

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With graduation approaching, Dr. Crowler begins to revert to his old ways, and Jaden Duels him to find out why.

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Duel Academy's Graduation Duels begins, and Jaden Duels a second-year student named Daigo Sorano. Meanwhile, Trueman's attack begins in Domino City, where he begins absorbing residents into the World of Darkness.

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Axel finds himself Dueling Trueman, who uses psychological warfare and hallucinations to create darkness in Axel's heart, while taking the appearance of Axel's own father.

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Jaden is saved from Trueman by Sartorius, but the latter is only part of the plot, being forced to Duel Jaden in order to save his sister, Sarina.

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Jaden's Duel with Sartorius continues, with the latter intent on saving his sister, Sarina

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Jaden is hallucinating, but begins to make his way back to Duel Academy. On the island, Trueman has taken the appearance and Deck of Daigo Sorano and is using them to defeat various students, continuing his siege, and absorbing people into the World of Darkness.

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Trueman's siege continues, and the entire school, save for Atticus is absorbed into the World of Darkness. In an attempt to free them, Atticus confronts Nightshroud.

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Atticus continues his Duel with Nightshroud as the latter reveals he has possessed Yusuke Fujiwara.

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Nightshroud begins a Battle Royal with Jaden and Jesse, attempting to turn Jesse against Jaden. Jaden vows to save Yusuke Fujiwara from Nightshroud on behalf of Honest.

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Jaden and Jesse continue their Duel against Nightshroud to save Yusuke Fujiwara. Nightshroud uses Trap Cards to manipulate the attacks and attributes of his opponent's monsters, while Jaden and Jesse narrowly avoid defeat after defeat.

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Jaden appears to be the last remaining human on Earth, with only Pharaoh and the spirit of Professor Banner for company. Nightshroud reveals his true form, as well as the origins of the universe. Jaden and Nightshroud begin their final confrontation.

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Jaden continues his confrontation with Nightshroud as the latter finds a way to counter Jaden's "Neos Wiseman". Those trapped in the World of Darkness begin to gain their memories and emotions back as Jaden attempts to find a way to prevail.

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Jaden attends his graduation ceremony and ends up traveling back in time, where he Duels Yugi Muto when he was at his strongest - just after winning the Battle City tournament and acquiring the Egyptian God cards.

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Jaden returns to Domino City and faces The King Of Games himself, Yugi Muto (or is it Yami Yugi in Yugi's flesh?).

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