During an era of rapid industrial growth, humanity is beset by the emergence of a mysterious virus, capable of turning humans into mindless creatures called "Kabane." With a desire for nothing but human flesh, these undead beings can only be killed by destroying their hearts—which are encased in a cage of unyielding iron.

Faced with such a dire situation, the surviving population has retreated into fortified cities known as "Stations." Isolated from the surroundings by massive moats and towering walls, the only contact with the outside world and other Stations is via a drawbridge for armored "Hayajiro" trains. At Aragane Station, Ikoma works as a steamsmith to maintain the city's active transportation. Despite his role, he is angered by mankind's cowardice and inability to repel the Kabane.

Utilizing his free time and knowledge as an engineer, Ikoma has created a new weapon to ward off the horde. An opportunity to test it presents itself when the Kabane invade Aragane Station, yet this encounter will prove to be much more than just a trial run for Ikoma.

During the first week of Japanese theater screenings for Koutetsujou no Kabaneri Movie 1: Tsudou Hikari, audience members were gifted a drama CD titled Hanashi Geki Koutetetsujou no Kabaneri: Shigure no Yume, which features a story that occurs after the TV series.