The Demon Train makes its first appearance just after the Tower of Spirits is split apart due to the disappearance of the Spirit Tracks, where it swoops down upon Link, Princess Zelda, and Alfonzo. The three are confronted by Chancellor Cole and Byrne soon afterward.
The Demon Train does not reappear until after Malladus is resurrected within Zelda's body, where the villains use it to make their escape from the top of the tower. Once Link has completed the Sand Temple and acquired the Bow of Light, a renegade Byrne reveals that he helped Cole create a Compass of Light as the only thing that could pinpoint the location of the Demon Train. Recovering the compass from its hiding place beneath Malladus's altar, Link and Zelda discover the way into the Dark Realm, where they manage to disable the Demon Train and climb atop it for the confrontation with Cole and Malladus.
By purging the Demon King from Zelda's body, the Demon Train is brought to a crashing halt and subsequently breaks apart, with the heroes and villains being ejected from the Dark Realm and sent back to Hyrule. The train's final appearance is in pieces surrounding the area where the final battle with Malladus takes place.
The battle with the Demon Train takes place on four adjacent sets of rails, with it taking up two of them due to its massive size. Link must navigate the tracks carefully to avoid a collision with the Demon Train as well as with the dark fire that obstructs his path on occasion. There is also only a limited amount of time in which the Demon Train must be defeated before the tracks come to an end, at which point the Spirit Train will plummet into the darkness below.
The Demon Train has two cars being towed behind its engine, all three of which must be disabled in order to defeat it. The rearmost car contains five compartments that open up to deposit explosive barrels onto the tracks in front of Link. These barrels must be detonated with the cannon before they leave their compartments in order to deal damage, with each compartment taking two hits. Once all of them have been destroyed, the Demon Train creates a portal leading back to the start of the tracks, leaving the disabled car behind.
The second car features four compartments that contain laser cannons that will fire on the tracks, attempting to damage the Spirit Train. Shooting each cannon once will disable it and switch to another, while two shots will destroy it completely. As before, all four laser cannons must be destroyed to disable the car and move on to the third phase.
The third and final phase of the fight pits Link against the engine of the Demon Train. As the hero comes up beside it, a series of cogs along its sides will arrange themselves and shoot out lasers in random directions. Destroying all of these slows the Demon Train and allows Link to get in front of it, where he must pound at its face with cannon fire. Repeating this process once more will stop the Demon Train in its tracks, allowing Link and Zelda to climb aboard.
- In real life, the Demon Train would be classified as a 2-8-0, having two leading wheels and eight driving wheels, known commonly as a Consolidation. This type of locomotive was used in the United States for freight service, and was discovered to be more powerful than older types of locomotives, fitting nicely with the locomotive in the game.
- The Demon Train, unlike the Spirit Train's more British design, resembles larger classes of American steam locomotives, such as the Union Pacific Big Boy.