The Village of Fragrant Blooms is being attacked, and the Big Four Mistress Beerain is behind it. Disguised as a young girl "Raine", Beerain tricks Igneous and Corona into smelling the Blossom of Darkness, which Hunter ultimately destroys, reversing the effect.

The Hill of Champions holds a monument where the Spirit Oracle first enshrined the first King Arachna with a Manacle. Buguese, the leader of the Big Four destroys the monument, expecting to find something. Hunter and Corona defeat Buguese's monster, but Buguese escapes with the timely intervention of a mysterious girl.

Buguese's loss to Hunter and Corona amuses Grasshop, who decides to prove his superiority by defeating the Spider Riders. However, Sparkle's creativity leads to Hunter's success in defeating the Invectids.

The Village of Fragrant Blooms is being attacked, and the Big Four Mistress Beerain is behind it. Disguised as a young girl "Raine", Beerain tricks Igneous and Corona into smelling the Blossom of Darkness, which Hunter ultimately destroys, reversing the effect.

The Hill of Champions holds a monument where the Spirit Oracle first enshrined the first King Arachna with a Manacle. Buguese, the leader of the Big Four destroys the monument, expecting to find something. Hunter and Corona defeat Buguese's monster, but Buguese escapes with the timely intervention of a mysterious girl.

Buguese's loss to Hunter and Corona amuses Grasshop, who decides to prove his superiority by defeating the Spider Riders. However, Sparkle's creativity leads to Hunter's success in defeating the Invectids.

Lazy Prince Lumen is asked to defend a village from the Invectids, but he makes a deal instead. At first the Invectids promise that they will settle in their own village and never attack. The Invectids attack again, and Lumen fights back.

The Forest of Bewilderment holds a secret and Hunter falls into it, supposedly never to return. Here he finds a Spider Rider named Magma, who is searching for a purple Spider named Portia. Hunter manages to leave the forest with Magma's help while Magma vows to join the other Spider Riders once he finds Portia.

Beerain escapes from Mantid and tries to find Buguese to inform him of Mantid's true intentions, but is attacked by Aqune, who damages Beerain's wings. Hunter fights Buguese and traps Corona to protect her, believing that Corona no longer wishes fight.

Grasshop and Sparkle find a badly injured Beerain and treat her injuries. Hunter and the Spider Riders consider negotiating with Invectids instead of fighting them. When Buguese appears, Hunter makes the offer, but ends up in a duel with Buguese instead. Beerain arrives to reveal Mantid's plan, but Buguese deliberately rejects her, aware that Mantid's spies are watching, and leaves her with the Spider Riders.

Despite Grasshop's request she stay, Beerain leaves the Spider Riders, uncertain where she will go, because she does not trust humans yet. The Spider Riders and Grasshop decide to infiltrate Mantid's castle through the dangerous labyrinth. However, when they are attacked and Hunter falls from a bridge, he awakes in the company of Aqune, who takes him to meet Mantid for the first time.

The Spider Riders try to think of a plan to find Hunter and get out of the labyrinth. Mantid reveals to Hunter how the Invectids have lived in darkness without sunlight for most of their lives and offers to prove it by removing Aqune's mask and having her show Hunter around.

Hunter agrees to give Mantid his Oracle Keys so long as the Invectids never attack Arachna again. Quake arrives and reveals to Hunter that Mantid is the one responsible for taking the Oracle Sun from the Invectids and that he has no intention of bringing it back. Corona and the others are able to leave the labyrinth at last and join Hunter and Quake.

Quake reveals a prophesy concerning eight Spider Riders defeating Mantid and that Quake (after Aqune rejoins them) is the eighth. Mantid gives Buguese control of his new creation, Dark Opal, and commands him to attack the Spider Riders with Aqune. However, when Hunter, after failing to reach a peaceful resolution, tries to use his Oracle Keys, their power is stolen by Dark Opal and given to Mantid, who is using Aqune to prevent Buguese from betraying him.

Mantid uses Aqune to steal the Oracle's power causing the Oracle herself to weaken and then enhances Aqune in order to have her defeat the Spider Riders. Mantid then shows up as his renewed self. Mantid then commands the spider riders to bow down to him Hunter trys to object but Grasshop doesn't let him. Grasshop tells Mantid to do what ever he wanted to do with him if he spare the spider riders. Mantid almost kills grasshop but is stopped by Buguese who order him to keep the promise he made to his people. Buguese then attempts to take Mantid on using Dark Opal, but is defeated. Mantid sends Aqune to attack the spider riders,then Buguese freeing Aqune from Mantid's control,.

Buguese survives after crashing Dark Opal into Mantid's fortress and laments that he lacked the power to force Mantid to bring back the sun. Grasshop guides the Spider Riders through the sewers to reach Mantid and the group separates again: Sparkle and Lumen escort Grasshop to visit his family, Igneous and Magma fend off Invectids, and Hunter, Corona, Aqune, and Quake confront Mantid, who reveals he was once an Earthen like Hunter and then summons a ship composed entirely of the Oracle's power - the Ark of Destiny.

Mantid intends to use his Ark of Destiny to ascend and conquer the Outer World with the Oracle's power and to take revenge on the Oracle, to whom he dedicated his life to only to lose the one he loved most in the process. Quake reveals his true power as a Spider Rider at last and the Spider Riders combine their efforts to destroy the Ark of Destiny. Buguese, after being rescued by Beerain and Stags, finds hope when he discovers the two abandoned Oracle Keys still glimmer with a faint light.

All hope seems lost for the Spider Riders as Mantid revives his Ark of Destiny and moves to strike them again with its power. Once Buguese delivers the two keys, Hunter uses the combined power of all four Oracle Keys and destroys the ark. Corona and Aqune watch with sorrow and fear that Hunter is using the Oracle's power with hatred, but the Oracle herself appears at last. She grants Mantid's final wish to become human again and reunite with his lost Loraine, Quake's spirit moves on with the Lost Mariner, while Hunter and his friends happily head toward their next adventure.

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