After finding a sacred talisman called a Manacle, Hunter Steele enters the Inner World through a portal deep within a pyramid. Here he meets Corona, a Spider Rider, and Shadow, a battle spider destined to be Hunter's partner.

Hunter and Corona are on their way to Arachna Castle, the home of the Spider Riders. On the way, they must save a village being attacked by Invectids led by Grasshop of the Big Four.

Hunter and Corona arrive at Arachna Castle, and Hunter meets Igneous and Prince Lumen. Hunter must prove that he is a Spider Rider in a duel against Igneous.

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.

Hunter is given a day to relax and decides that he wants sleep. Unfortunately, everyone else thinks he should be doing something else and won't leave him alone.

When a village is disrupted by Invectids digging a tunnel to reach the Oracle's shrine, Hunter and Aqune are separated from their respective groups. While Hunter's friends look for him, Aqune takes care of Hunter until Buguese arrives.

While Grasshop is assigned to distract the Spider Riders using whatever means possible, Buguese searches for the Oracle Keys. Grasshop challenges Hunter, Corona, and Igneous to an elaborate duel, but attempts to end it with a giant Invectid mech. Magma arrives to save the day while Buguese and Aqune successfully break into the shrine holding the first of four Oracle Keys.

Grasshop accidentally reveals Lord Mantid's plans to acquire the Oracle Keys and the Spider Riders must rush to the Oracle's shrine to recover the key before Buguese does.

With the Oracle Key in hand, Hunter and Shadow become more powerful warriors. However, they find that even with their newfound abilities, they still cannot free Aqune and Portia from Buguese's control.

Stags has heard of Hunter's new power and wants to try and defeat it by challenging Hunter to a duel. However, Hunter finds that he cannot summon the Oracle's power at will until he is in true danger. The Spider Rider defeats Stags, who vows return someday to defeat Hunter.

Legend says whoever sees a shadow of a dancing spider will be cursed, unless the person sees the shadow again (which will remove the curse). Hunter sees the shadow, then Igneous and Magma, then Corona. However, it is revealed that the shadow is more friend than foe and not a ghost at all.

Lumen sends Corona and Hunter to search for the second Oracle Key in Araja Village, which happens to be where Corona was raised. Beerain follows them in hopes of snatching the key away and a battle between the Invectid and the Spider Riders ensues.

Slate, an old friend and comrade of Igneous, returns to Arachna for a visit. Hunter is dismayed that the former duo are not getting along, especially when Slate challenges Igneous to a duel to prove their strength, only to discover that Grasshop is blackmailing Slate.

Hunter and Magma find a maskless Aqune in an ancient school with no knowledge of how she arrived there; a suspicious Magma believes Aqune could be a spy. He and Hunter must soon battle her and Portia, who declares her brother Brutus is an enemy, when Buguese arrives to take back Aqune.

The Spider Riders have been facing Invectids everyday for weeks now and Corona is tired of fighting. Castle seer Lily offers to show Corona what her life would be like according to the Spider Rider's dreams.

Hunter accompanies Magma, who is travelling to a nearby village to find more information on Portia. Hunter meets Katy, an Invectid who lives among humans because she does not believe in fighting. She is captured by Grasshop and Aqune.

The city of Nuuma is under siege by Stags, who seeks to claim the Oracle Key enshrined there. The Queen of Nuuma sends a page to deliver a mysterious box to Arachna Castle, but ends up dropping the box on Lumen's head. Chaos ensues as the Spider Riders attempt to save the page while Grasshop attempts to take the box.

The page from Nuuma reveals his box contains another Oracle Key and that Stags has invaded Nuuma. While Hunter believes they need to go to the faraway Nuuma, Lumen refuses because it would mean leaving Arachna defenseless for a long period of time. Meanwhile, Beerain and Buguese are sent to retrieve the two Oracle Keys now in Hunter's possession.

Grasshop disguises himself as a woman, believing he'll be able to sneak into Castle Arachna to steal the Oracle Keys. The plan, like most of Grasshop's, goes awry and the Invectid is soon dismissed by from the Big Four.

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.

Hunter discovers that the Invectids have invaded the city of Nuuma and wants to go help the Nuumans, but is disappointed that the other Spider Riders are reluctant, even with the possibility of a third Oracle Key being there. Grasshop appears again with the unstoppable Goldenbore to steal Hunter's Oracle Keys; can the Spider Riders create an opening so Hunter can defeat this foe or will Buguese and Aqune turn victory into defeat?