While The Quiet War and Gardens of the Sun were set in a mid-term future Solar System, In the Mouth of the Whale is spatially and temporally much further out, set thousands of years in the future around a Fomalhaut system long since colonised by refugees from the Quiet War. The first settlers, the Quick, have since been superseded by the True who are in turn challenged by the posthuman Ghosts.
The story is told from the point of view of three characters. The first, the Child, believes she lives in a village in the conflict-torn Amazon. She becomes transfixed by a mysterious boy with the head of the jaguar but in reality, her world is part of an elaborate, failing, simulation created on a damaged starship that is finally on the verge of reaching Fomalhaut. The crew created the simulation based on her experiences of life before the Quiet War and hold her in high regard, however, those already at Fomalhaut know of her impending arrival.
The second, Ori, is one of the Quick. She remotely pilots maintenance spacecraft around the Whale space station, which orbits the gas giant Cthunga. The Whale station is attempting to make contact with a mind which had crashed into the planet long ago and is thought by the True to have transcended. It is Ori who witnessed what could be a sign from the Mind, which quickly attracts the attention of the True.
The third strand is the Librarian, who with his assistant Horse kills demons to atone for having caused the death of two of his comrades. These "demons" are the corrupted remains of Quick technology but when he is faced with a mission which parallels the tragedy from his past, he begins to see a way in the Library itself. These three strands converge as the Ghosts and True are drawn inexorably into conflict.
