Stags and his army are about to obtain the fourth Oracle Key when the Oracle raises a shield around Nuuma Castle and raises it into the sky. Hunter continues to try and convince the other Spider Riders to go to Nuuma; fortunately, with Slate's return to Arachna, none of the Spider Riders have any reason to refuse to go to Nuuma.

The Spider Riders reach the town of Fuushuwa and discover they need to a ship in order to sail up Fuushuwa Falls and then across the Inner Ocean to Nuuma. When Quint, owner of the only ship in town, refuses to help them, Hunter tries to find his own way to Nuuma.

The voyage to Nuuma is anything but pleasant - the Spider Riders are disorganized, getting seasick, the food is disgusting, and everyone is lazy. Hunter's efforts to put everything in order are in vain and things only get worse when they find they have to somehow cross a channel of lava.

The Spider Riders are attacked by Invectids but lose them when their ship enters a strange fog. A mysterious ship appears before them and they meet the Lost Mariner, a sailor who once aided the hero Quake on his way to Nuuma.

With their ship is destroyed, the Spider Riders are separated and Hunter, Corona, and Magma wake up in a strange forest. Aqune appears and is prepared to attack when her mask crumbles and she and Portia are released from their spell. Buguese arrives to retrieve Aqune, Portia, and Hunter's Oracle Keys, but everyone suddenly disappears, leaving Buguese confused. The Spider Riders are in a place where they are offered the decision to give up their lives as Spider Riders and live peacefully. Will Hunter and the other Spider Riders throw away their manacle's to live peaceful lives?

Hunter and the Spider Riders are back in the forest where they come upon a strange old man who claims that he is the hero Quake. The man's identity is in doubt until he successfully fends off Buguese and his Invectids with his staff. Quake then sends the Spider Riders on their way, by opening a portal to the desert.

Lumen and Igneous are travelling across forested land when they find Sparkle, who reveals she has been accompanied by her "Uncle Hop" - Grasshop. Grasshop must decide if he wishes to continue aiding the Invectids or help the Spider Riders, especially Sparkle, who reminds him on his own children and whose kindness has saved him more than once.

Both Corona and Aqune have unsettling feelings concerning what will happen in Nuuma. Buguese arrives and captures an injured Corona to use her as bait to take Hunter's Oracle Keys. When Hunter agrees to give up the keys for Corona, Buguese reveals his true plan - to regain control of Aqune. The Spider Riders are finally all reunited.

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 fights Buguese's Battle Beetle, but cannot defeat it until Grasshop helps out by removing its regeneration component. However, Buguese reveals that he was merely distracting the Spider Riders while Aqune removes the Oracle Key from its chamber.

With the Oracle Key removed, Nuuma Castle starts falling to the ground. Hunter and Corona use the Oracle's power along with one of Hunter's Oracle Keys to bring the castle down safely. Queen Illuma reveals startling details about Corona's and Aqune's past as being sisters as well as being handmaidens to the spirit Oracle.

Upon returning to Arachna, the Spider Riders discover Invectids at the castle. Slate and his troops struggle to hold them off until Igneous turns the tide in their favour. The Invectids flee, only to return at night with a new type of Invectid to attack Slate and other guards.

Mantid, with two Oracle Keys in his possession, creates a cannon capable of attacking Arachna Kingdom. Hunter and Corona sneak into Mantid's fortress to disable the cannon while Beerain discovers Mantid's true plan - to take all of Oracle's power for himself and with no intention of bringing sunlight back to the Invectids' land.

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.