Adventurous teen Hunter Steele follows his grandfather's directions in search of a doorway to the Inner World. Deep inside an ancient pyramid, Hunter acquires a unique manacle and falls into a new and frightening land deep within the earth. Hunter is almost killed by a giant, talking spider named Shadow until the unlikely pair are forced to team-up as Spider and Rider to combat the Invectid forces of the evil Mantid. But will their uneasy alliance survive the battle?

Hunter gets his first lesson in being a Spider Rider from Corona as they travel deeper into the heart of Arachna. But soon Hunter insults Shadow and it looks like their partnership may be over before it starts. When the evil Grasshop threatens to destroy an Arachna village, Hunter rushes to face the challenge alone, despite his inability to summon his powers. Will Shadow unite with Hunter again or will he let the newest Spider Rider pay for his mistake with his life?

Hunter Steele finally arrives at Arachna Castle and quickly makes a bad impression on his fellow Spider Riders; especially the disdainful Igneous. Forced to prove themselves, Shadow and Hunter enter the arena to show Igneous what they're made of. But the veteran Spider Rider and his Battle Spider, Flame, prove to be an unstoppable force. If Shadow and Hunter can't find a way to work together, they may never discover their true power.

Hunter is quick to volunteer when the Village of Fragrant Blooms calls on the Spider Riders for help against an Invectid assault. Corona and Igneous are overwhelmed by the beauty of the flowers the town is famous for but Hunter is too keyed up to notice. The trio find the village abandoned save for one little girl, Rain. Seeking the villagers, they follow her directions to a cave in which the Blossoms of Darkness grow. The Blossoms turn Corona and Igneous into enemies until Hunter and Shadow destroy the flowers. But it's not until Hunter literally stops to smell the roses that he is able to help his friends and the village overcome an attack by Beerain's drones. There truly is strength in beauty.

Corona takes Hunter to the Hill of Champions; the place where spiders and humans first fought together against the Invectid invaders. They meet Galena, a woman whose Spider Rider husband disappeared many years ago. She cares for the monument while awaiting his return. When Buguese arrives to claim the hill, Galena shocks the Spider Riders by giving it up without a fight. Despite Galena, Hunter and Corona defeat Buguese only to find themselves thrown back by his human ally, Aqune! Through Galena's courageous example, the Spider Riders learn the things that are truly worth protecting lie not in stone monuments, but rather within our hearts and spirits.

Every child in the city is playing with a sparkling sphere but Princess Sparkle. After Hunter discovers where the children found the spheres and gets one for her, Sparkle is afraid to tell him that it turned black when she tried to paint it. But when Grasshop invades the city by controlling the children with his spheres, Sparkle's mistake saves her from its hypnotic effects. The spheres form a giant robot that uses the children as a shield and warps light, rendering it invisible as it pummels Hunter and Shadow. It's only when Sparkle and Hunter realize her black sphere remains visible even when the rest of the robot is not that they are able to turn the tables. And so Sparkle, the youngest Spider Rider, achieves her first victory over the Invectids with the help of Hunter, the newest Spider Rider!