At the massive spaceship Sidonia, having exhausted his last supplies of food, Nagate Tanikaze ventures outside home to look for food when he is spotted and captured by the local security while trying to steal some rice. Believing that his life is at risk, Nagate manages to escape the hospital where he is being treated just to be apprehended by some military cadets. One of the cadets, Shizuka Hoshijiro, accompanies Nagate while he is being questioned by the police, when a man called Ochiai appears and takes him to Captain Kobayashi, the highest authority of Sidonia, who claims that she intends to take him under her guard, with the condition of becoming one of Sidonia's Guardian pilots, to which he accepts. He is then registered as an official cadet and introduced to the others. In the occasion, Nagate learns that the Guardian pilots' main mission is to defend Sidonia against an alien hostile species known as the "Gauna", although the last time they encountered them was a hundred years before, and befriends Izana Shinatose, an hermaphrodite whose body can be adapted to procreate with either males or females, depending of the chosen partner. After failing to impress his peers at the pilot simulator, as the controls are different from those he trained to perfection at his former home, Nagate is called to his first sortie along Shizuka and Izana, but instead of piloting one of the recent Type 18 models, Nagate is entrusted with Tsugumori, a legendary Type 17 unit that belonged to a famous war hero, much to the anger of Norio Kunato, a cadet who always wanted to become its pilot and is being dispatched with him as well. Realizing that Tsugumori's controls are similar to those he is used to, Nagate's confidence is renewed but while performing a mining operation at a nearby asteroid with the others, a Gauna appears from inside it and attacks them.