Eleven-year-old Hunter Steel searches for the legendary inner world by following the instructions in his grandfather's journal. He enters a cave where he finds a mysterious manacle that attaches itself to him. A spider startles Hunter, who falls into a hole to the center of the Earth and into the subterranean world of Arachna. There, he discovers a small group of elite warriors struggling to survive and to save Arachna from the attack of giant insect mutants. The warriors are children, each fighting with the help of their own 10 ft (3.0 m) battle spiders. They call themselves "Spider Riders". In the English TV series, the ages of the characters were reduced. ... There is a prophecy that says a surface-dweller or Earthen, like Hunter, will bring disaster to the Inner World. Sparkle mentions it in the beginning of the TV series. When Princess Sparkle finds out she says, "I wonder if he will bring doom to us...or to them."

The Oracle Keys are fractions of the Oracle's power. They are cards that can be split in two. The Invectids hope to gain them for Mantid, who wants to use their power to rule Arachna. The Oracle uses much of her strength to protect them. The Spirit Oracle Key passes its power onto Hunter and Shadow, giving them new armor and weapons as well as new abilities.

To activate these keys, the holder must shout "Oracle's Light!". Two in combination can create more powerful armor and weapons. The wielder must have a sincere desire to protect without arrogance, otherwise the keys will not work. The Oracle Key from Nuuma was called by Corona, using her power, to let Hunter use it without having to hold it. Mantid used two of the Oracle's keys to power himself, plunging the Inner World into darkness and preventing Hunter from using his own keys.

Currently the locations of the four Oracle Keys are known in the English version:

Found in the Oracle's shrine in Arachna, the first key is taken by Hunter and Shadow, who retain possession of it throughout the series.

The second key is brought to Arachna by a page from Nuuma. Hunter and Shadow have it in their possession for most of the series, though it was briefly taken by Aqune and Portia.

The third key is initially kept in a sanctuary in Nuuma and allows the castle to float in the sky via the Oracle's power. It is taken by Aqune for the Invectids, but ends up in the possession of Hunter and Shadow during the final battle against Mantid.

The fourth key held by Mantid powers Castle Mantid and sustains Mantid throughout the series until he steals the Oracle's power and abandons it. It ends up in the possession of Hunter and Shadow during the final battle against Mantid.