Olly Appleton thought he had learned all of his grandfather's secrets, the ones his grandfather died protecting. Those secrets involved hand-drawn maps, special keys, hidden tunnels, and the Spores-friendly and fantastical mushroom creatures living under his home on Oak Hill. With his friend Ember by his side, Olly learns of another secret. Other Spore communities are being built around the country in towns that share the name Littleton. The latest community is Sapphire Creek, an abandoned gold mine his grandfather purchased outside Littleton, Colorado. When Olly's parents plan a surprise trip to visit the property, he and Em decide to share all of the secrets with their families at a special feast in the Spores' Grand Cavern on Christmas Eve.

And when Sapphire Creek comes under attack, Olly and Ember once again team up with their Spore friends-and some unlikely friends-to defend the community without exposing their secrets to the outside world.