The beautiful adventure game The Whispered World whisks the player away to a fascinating fantasy world. Sadwick is a young clown but often far from cheerful. One night, a strange blue creature speaks to him in a dream, and sends him on an adventurous journey.

In classic point & click tradition, gamers steer Sadwick and his companion Spot through the game. Little Spot never leaves Sadwick's side and is integral to solving many puzzles. He can take on many different forms throughout the game, which the player can pick and choose at will, once they have been learned.

The game takes place in Silentia, a dream fantasy world, that is the home of a young, sad circus clown named Sadwick. The story starts as he wakes up in his travelling circus trailer after having experienced a recurring nightmare, where he sees the world falling apart.

Sadwick goes for a walk in a nearby forest and meets Bobby, a Chaski, messenger of the King. Bobby is heading to Corona, the royal castle, to deliver a powerful artefact, the Whispering Stone, to the king. He claims the end of the world is near and the land is already breaking apart and that the Asgil, a hideous horde of underground creatures, are surrounding Corona. He tells Sadwick that he has been unsuccessfully seeking out an oracle named Shana for advice on shortening his trip, and he asks Sadwick to help him find her. Sadwick believes that maybe she can interpret his nightmares, and he convinces Bobby to give him the Whispering Stone to help him find the oracle. Shortly after Bobby gets scared away and disappears in what Sadwick believes was an Asgil attack. Sadwick finds a secret passage that, when activated by the Whispering Stone, leads him to Shana, and finds out from her that his destiny is to destroy the world.

Shana directs Sadwick to a nearby island to find mysterious Kalida who eventually takes him near Corona. There Sadwick comes across the Asgil hideout and manages to listen in to the plans of Asgil leader Loucaux but gets captured and thrown in a jail cell. After successfully escaping, he manages to board a flying steam locomotive to Corona, where he meets Bobby again who tells Sadwick that he is too late and the king has locked himself in his quarters. Exploring the castle, Sadwick finds a model of a planetary system linked to the flow of space-and-time itself. He meets the royal astronomer who tells him the Whispering Stone represents the planet Silentia in the model of 5 planets and the king must repair the system to restore the balance, but he has fallen ill, and only when the system is repaired can it activate the fountain of the Water of Life that can wake the king.