Gameplay in Myst III: Exile is similar to that of its predecessors. The player explores immersive, pre-rendered environments known as Ages by using either mouse clicks or the space bar for movement from set nodes across each Age. Unlike previous games, which employed a series of still images, Exile uses a "free look" system which gives the player a 360-degree field of view. The game also has an optional Zip mode, like Myst and Riven, to cross explored terrain quickly by skipping several nodes. Clicking allows the player to manipulate objects and pick up items. The on-screen cursor changes in context to show possible actions.
Each of the game's Ages has a distinctive look and theme. Players begin their journey on the Age of J'nanin, which acts as a hub linking to other Ages and as a "lesson Age" demonstrating important principles for later puzzles. Three of these Ages are Amateria, a mechanical Age in the middle of a vast sea; Edanna, a world of preserved nature, with abundant plant and animal life; and Voltaic, a dusty island riddled with canyons filled with man-made constructions.
By gathering clues and manipulating the environment, the player solves thematically linked puzzles. For example, the book leading to Voltaic is accessed by aligning beams of light across a canyon; the Age itself contains similar energy-based puzzles. Edanna's plant-filled puzzles require manipulation of the Age's ecosystem. Puzzles often involve observing interactions between elements of the environment, then adjusting the links between them. The player can also pick up and view journals or pages written by game characters which reveal back-story and give hints to solving puzzles. Cursor Mode allows the player to select items from a personal inventory at the bottom of the screen.
Exile begins 10 years after the events of Riven, when the Stranger arrives at the home of Atrus and his wife Catherine. Atrus is a scientist and explorer who has mastered an ancient practice known as the Art: he can create links to different worlds, called Ages, by writing special books. This ability is by an ancient civilization known as the D'ni, whose society crumbles after the D'ni city is devastated by a plague. Atrus calls the Stranger to his home to display his newest Age, Releeshahn, which Atrus has designed as a new home for the D'ni survivors.
As Atrus is preparing to leave for Releeshahn, a mysterious man appears in Atrus' study, steals the Releeshahn book and leaves behind another. Following the thief, the Stranger arrives at J'nanin, an Age that Atrus had written long before as a way to teach the Art to his sons. Because the thief has caused considerable damage to the J'nanin book, Atrus cannot accompany the Stranger.
The mysterious man is named Saavedro. Twenty years earlier, Atrus' wayward sons Sirrus and Achenar destroyed Saavedro's home Age of Narayan and trapped him on J'nanin. Saavedro believes his family is dead and swears vengeance on Atrus, unaware that Atrus has already imprisoned his sons for their crimes and that Saavedro's family is still alive. The game can end several ways depending on the player's actions. In the most ideal scenario, Saavedro returns to Narayan peacefully after giving back the book of Releeshahn. Other endings result in Saavedro destroying Releeshahn or killing the player; another option allows the player to leave Saavedro trapped forever.