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The story begins with the voice of Darktail guiding the player through the levels. While he's imprisoned, he tells the player to free him along with an Earth Gemling named Tyranticore who is an alternative of Manticore. Tyranticore defeats all the Gem Guards on the way, including the Brick Golem. The player and Tyranticore break out Darktail, and he tricks the player. Tyranticore is overheard to have made a deal with Darktail, that he will get his reign along side of Darktail. The black fox, takes away the Rainbow of the castle, and fills the places with Dark Sludge. Rainbowtail then guides the player through the rest of the levels, saying that he saw the whole thing and that the player was tricked. He tells them to go to King Bean who gives them their starter pet randomly out of three choices. Frooma, Groma, and Durgo. At the first boss level, the Brick Golem tries arresting the player for releasing Darktail but once defeated, he claims that they will be caught. The journey continues to Mellow Meadow.
Snoodle, a little mouse, notices the Sludge and the gems that are protected by Bone Jail. After the level is beat, Snoodle finds out the player let Darktail out but forgives the player for clearing the sludge and fixing the problem. But the Brick Golem once again catches up to the player and brought Gem Guards along. The Brick Golem is defeated, as Rainbowtail cautions the player and the journey continues to Sacred Forest.
Rainbowtail spots a Floferry, one of the guardians, who warns the player about easily getting lost in the forest. But after they beat the level, Floferry recognizes the player from a legend. She says that an Almighty Gem Mover would restore balance of the the Rainbow Castle as well as the others. The guardian of the forest, is another Brick Golem who tries capturing the player but when they beat him, he is angered that they are blessed by gem spirits. The journey continues to Pondside.
Bubrog comments on the Dark Sludge. He asks you to cleanse the pond. He also says that it's not normal Dark Sludge and that it's Dark Sludge+ which you have to clear twice. At the level before the boss level, he guides you to the last part of the ponds pollution. After the Dark Sludge is cleared, Bubrog thanks you and tells you there is a big guy waiting for you. It turn out to be the Brick Golem angry at how hard he has to run and catch you. Once again angered, he yells at his defeat and you make your way to Driggle's Cave, and the Brick Golem does not catch up to you.
Driggle welcomes the player cheerfully but tells them about the spider problem and asks them to get rid of the spiders. The Aracnabean shows up and says that he wants to stay there saying also that gems won't bother him. Once defeated, Driggle bows down to the player and refers to him as the Almighty Gem Mover.
Nobril, a pet, asks if you pursue the Most Notorious One. He then warns you that you may want to go back and level your pets as strength comes through preparation and not power. He tells the player to be cautious in the Field, because now, Aracnabean rules over it. After the giant spider is defeated, the journe continues in to Dead Woods.
Cactodon, a pet, informs you that this is not the first time Darktail has been set free. He doesn't believe you will be able to be the hero. At the end of the level he believes you may be right for the job and goes back to sleep. Throughout the Dead Woods Rainbowtail begins to show fear and doubt because Aracnabean is trying to kill the player After the boss level Rainbowtail tells the player that he wasn't sure you were going to make it and is impressed that they did. The make your way to the Stony Watchtower.
Darktail is seen trying to mock the player about getting lost and makes his escape. After the level is beat, Rainbowtail shows up apologizing that he is late that he was held back by spiders. At the boss, Aracnabean states, "Are you lost child? You can stay here with me...Forever." But once defeated, Rainbowtail is beyond impressed. But also says Darktail already escaped and they must continue onward.