Shade's position as oft-teased runt causes him to take a major risk, breaking an ancient law that forbids bats from flying in the daylight. As a result of Shade daring to see the sun, the owls anger is roused, and they burn down the bat's roost, forcing the colony to embark on a premature migration.

Shade meets up with fellow outcast, Marina Brightwing, after becoming separated from the Silverwing colony during a storm. The two decide to try to meet up with the Silverwing colony together. Meanwhile, captured in the jungle of their South American homeland, two vampire bats, Goth and Throbb, awake in a human laboratory. Clever and resourceful, Goth quickly hatches a plan to escape through the ceiling vent.

Goth and Throbb celebrate their escape, by dining on pigeon, before making their way south. When Shade and Marina enter the city, they are captured and interrogated by pigeons seeking vengeance over the death of one of their own at the jaws of a bat.

Shade and Marina meet Zephyr, a mystical Albino bat who serves as an oracle to the bat world, and gives Shade and Marina a hint of a great "prophecy". Lost in a strange land, Goth decides they need a guide for the unfamiliar skies, and meets up with Shade and Marina, saving the two young bats from an owl attack.

Mistaking Goth for a friend, Shade discloses the sound map containing the path to his colony's new roost, to Goth. Shade soon realizes the evil ways of his friends, however, when he comes across Throbb eating a Brightwing. Together, Shade and Marina plot their escape.

Shade is sickened that he has given Goth his colony's soundmap. Now, he and Marina race to the "Fire Tower" to save the Silverwing colony, and face battle with Goth and Throbb. Along the way, Shade and Marina make an unlikely ally in Orestes, the owl.