An editor's preface notes that after each telling of the legend the pups ask many questions:
The tales primarily focus around the Webster family, and their robot servant, Jenkins. The name Webster gradually becomes "webster", a noun meaning a human. Themes familiar to Simak readers recur in these stories, notably the pastoral settings, the faithful dogs, and Simak's unique idea of time. In these and other stories, there is no future or past. The Earth travels on a thread of time, and both behind and before it are other Earths, some quite different. To travel in time is not to go to the past or future, but to travel to one of these worlds.
Each successive tale tells of further breakdown of urban society. As mankind abandons the cities, each family becomes increasingly isolated. Bruce Webster surgically provides dogs with a means of speech and better vision. The breakdown of civilization allows wandering mutant geniuses to grow up unrestrained by conventional mores. A mutant called Joe invents a way for ants to stay active year round in Wisconsin, so they don't start over every spring. Eventually the ants form an industrial society in their hill. The amoral Joe, tiring of the game, kicks over the anthill. The ants ignore this setback and build bigger and more industrialized colonies.
A later tale tells of a research station on the surface of Jupiter. Simak's version of Jupiter is a cold, windswept, and corrosive hell where only advanced technology allows the station to exist at all. A scientist is accompanied by Towser, his tired and flea-bitten old dog. But there is a problem. Men permanently transformed to survive unaided on Jupiter's surface leave the station to gather data and inexplicably fail to return. Finally the scientist transforms himself and his canine companion into the seal-like beings that can survive the surface. They leave the station in their new form and experience Jupiter as a paradise. Towser's fleas and irritations are gone and he is able to talk telepathically to his former master. Like the previously transformed station personnel, the scientist decides never to return.
He eventually does return, to share with all humankind what he has discovered. It seems impossible - how can he show them the wondrous Jupiter that he and Towser perceive? Joe steps in again, once more out of sheer mischief. He knows a mind trick to allow people to broadcast meaning to others' minds as they speak. By means of a kaleidoscope-like instrument, he can twist the minds of other people so they can perform the mind trick. Thus all humanity learns the truth about Jupiter, and most elect to leave Earth, give up their physical humanity and live transformed on Jupiter's surface
Simak's vision of the apocalypse is unusual, not one of destruction, but simply of isolation. Much of humankind becomes so lonely that it eventually dies off. Some favor starting over as a completely different species capable of experiencing on Jupiter the simple bliss that humans have otherwise lost.
Ten thousand years in the future, Jenkins is provided with a new body so he can better serve the few remaining "websters". A wraithlike creature called a cobbly appears, having traveled from another world on the time thread. Before it is driven away, Jenkins's new telepathic sense enables him to read the creature's mind to discover how it moves from world to world. Realizing that humanity cannot peacefully coexist with the Dogs and other animals that are now intelligent and pacifistic, Jenkins uses the knowledge to take his human charges to one of the other worlds. Eventually the human race dies out on the new world.
Returning to the initial Earth in the final tale of the book, Jenkins finds the dogs dealing with the ever-growing Ant City, which is taking over the Earth. Jenkins travels to Geneva, where a last small group of humans sleep in suspended animation. He asks his former master, a Webster, how to deal with the ants. The answer is typically human - poisoned bait, enough to kill but not before the bait is taken back to the ant colony, so it is fed to the queen. Jenkins is saddened because he realizes the Dogs will never accept this solution. He tells the dogs that the "websters" had no answer. He and the Dogs leave Earth for one of the other worlds.
The stories were written in the post-World War II world, and reflect the attitude that humans are unable to live at peace with their fellow beings. There is an underlying theme throughout the book that humans possess a fundamental aggressive flaw they will never be able to overcome.