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Dragon Quest VI opens as the Hero, Mireyu, and Hassan approach Mudo, the demon king’s castle. After Mireyu summons a dragon, the party enters the castle and comes face to face with Mudo. Overpowering the trio, Mudo appears to destroy each member of the party. The Hero wakes up in Lifecod, and cannot remember anything before the fight with Mudo. Tania, a small girl from Lifecod, insists that he is her brother.
On his way to Reidock Castle, where information on Mudo can be found, the Hero stumbles into a strange portal which brings him to another unfamiliar town. However, no one can see or hear him. After finding a similar portal, the Hero reaches Reidock and meets Soldi, the leader of Reidock’s army, and Hassan, who appears not to remember the Hero. To defeat Mudo, they learn, they need the Mirror of Ra. The Hero and Hassan discover another portal, which brings them to San Marino, another town they can neither be heard nor seen. Mireyu, also appearing to have lost her memory, does see them and helps them become visible.
The party discovers a Reidock Castle in the “Phantom World” and learns that the prince is missing and that the Hero looks like him. They also meet General Tom, who bears a striking resemblance to Soldi. Gaining entrance to the Mirror Tower, the party meets Barbara, a woman who was invisible in the “Phantom World” at first, too, and together they find the Mirror of Ra.
The four of them travel to Mudo's castle, in the original world. After defeating Mudo, the Hero uses the Mirror on him. Mudo then turns into the king of Reidock, confused and unaware of what happened. The king reveals that the original world is in fact the Dream World and the Phantom World is the Real World. Upon traveling back to the Real World, the King of Reidock thanks the party for defeating Mudo in his dreams, but that the real Mudo lives and that the party must travel to Gent to retrieve a boat to get to Mudo's lair. In Gent, Chamaro, a healer, joins the party and allows them to use the Gent Clan's ship. During the fight with the real Mudo, the Hero gets sent back to Lifecod, like before. However, with the Mirror of Ra, the Hero warps back into the battle and defeats Mudo.
The Queen of Reidock tells the Hero to discover who he really is. The quest leads the party to Arcbolt, where a terrible monster is blocking a nearby cave. The reward for defeating the monster is the famed Sword of Thunder, but before the party can strike the final blow, a warrior by the name of Terry kills the monster, winning the sword. After traveling both worlds, the party learns that Mudo was not the only evil in the world, having fought several other monsters that all seem to be connected.
In Calberona, the party learns that this is Barbara's home. The elders tell Barbara that the Demon Lord is watching her and give her the powerful spell Madante to fight him. The party also learns that the only way to get to the Demon Lord is through Zenith Tower, but to activate the tower, they need to collect the sword, armor, shield, and helmet of legend. While doing so, the Hero meets his double in Real Lifecod. Returning to Real Reidock, the King and Queen tell the Hero that he is indeed the prince. When he fused with his clone, the Hero gained his memory back, much like Mireyu and Hassan had done.
The party reaches Cloud Castle and meets Duran, who claims to have taken over the castle. He summons Terry to fight the party and then fights the party himself. Duran then reveals that all the enemies the party has faced were just pawns of Deathtamoor, the Demon Emperor. Mireyu reveals that Terry is her brother and Terry decides to join the party and fight against Deathtamoor.
Once Cloud Castle is back to normal, the party speaks to King Zenith who informs them of Deathtamoor's doings and how to reach the Dark World. Deathtamoor plans on merging both worlds. The party’s horse fuses with Pegasus, allowing the party to fly to the Dark World. With the help of two brothers, Krimut and Masarl, the party enters Deathtamoor's Castle. After solving many puzzles, they come face to face with Deathtamoor and defeat him. Masarl reveals that the Dark World is falling apart and Pegasus helps them escape.
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