The story takes place a century after the events of Phantom Hourglass, in a new world where the “Spirit Tracks” — magical railway lines connecting sacred temples — begin to mysteriously disappear. Link, an apprentice engineer, is called to investigate the phenomenon and soon witnesses the attack of Chancellor Cole, who removes Zelda's soul from her body to be used as a vessel for the demon Malladus. Zelda, now in spiritual form, accompanies Link throughout the adventure, offering help with puzzles and battles.

Players travel by train between regions, face enemies, explore dungeons, and use the touch screen to solve puzzles. Cooperation with Zelda is a central element, as she can possess Phantom Armor and actively assist in overcoming challenges. The game stands out for its original use of the train as a means of transportation, the dynamic Link–Zelda relationship, and the utilization of the DS's capabilities, offering a fresh and exciting adventure in the world of Hyrule.