In a distant future, a false utopia known as Jesus Town stands behind imposing walls. Built on the site of what was once Jerusalem, the city is ruled by the seraphim-like dictator Gurjev and his powerful android enforcer, Michael. They maintain a brutal, sterile peace through fear, lobotomizing dissenters and any citizens who dare to exercise free will. Outside the city, a small band of leather-clad rebels struggles to survive, dreaming of overthrowing Gurjev's iron grip.

Their hope arrives in the form of a destructive force they may not be able to control. A group of treasure hunters breaks into an abandoned, high-security prison and discovers a man in chains. When they accidentally awaken him, he reveals himself to be the android Hakaider, a deadly combat unit known as the "Destruction Rider." He swiftly kills his rescuers and escapes on his black motorcycle, Guilty, heading toward Jesus Town. Hakaider's memory is fragmented, and he does not fully understand his own purpose or past, though it is hinted that he was Michael's failed predecessor, created by Gurjev but scrapped after developing free will.

Upon arriving at Jesus Town, Hakaider single-handedly smashes through the city's electric barrier and defeats a squad of security officers with brutal efficiency. His rampage is witnessed by a group of rebels, including a young woman named Kaoru. Unlike her cynical comrades, Kaoru is captivated by Hakaider, recognizing him from recurring dreams in which a knight in shining armor arrives to liberate her people. When Hakaider is temporarily knocked unconscious, the rebels drag him back to their hideout.

At the rebel base, Kaoru grows close to the silent, violent android, developing a romantic attachment to him. The rebels explain their plan to overthrow Gurjev, but Hakaider remains distrustful of their selfish motives. Their fragile alliance is shattered when Michael and Gurjev's security forces track them down. A vicious shootout erupts, and most of the rebels are killed. As Kaoru escapes, she watches in horror as the soldiers apparently destroy Hakaider with a rocket launcher. Wounded and grieving, she stumbles into the streets of Jesus Town, publicly condemning the citizens for their cowardly compliance with the regime. Michael finds her and delivers a fatal wound. Her final scream of pain resonates through the city, somehow reactivating Hakaider.

Hakaider finds Kaoru at her "secret spot," the last oasis in the dying city. She confesses her love for him and, dreaming of a peaceful future they will never share, dies in his arms. Taking her charm as a token, Hakaider rides back into the heart of Jesus Town, now fully embracing his role as an engine of destruction.

He storms the government building, wiping out the remaining security forces. When he encounters a group of citizens scheduled for lobotomy, he asks if they possess free will. When they answer yes, he frees them. He then confronts Michael in a brutal final battle. Michael argues that enforced order is justice, to which Hakaider replies that if that is justice, he will proudly be evil. Hakaider manages to decapitate the android, whose severed head continues to mutter "I am justice" as it sparks and fails.

Gurjev pretends to negotiate with Hakaider, stalling for time as Michael's head is integrated into a massive battle tank modeled after Kikaider, a heroic android from the past. In this new, monstrous form, Michael attacks again. Hakaider destroys him a second time using a concealed weapon. He then finds Gurjev, who desperately fires a revolver at him to no effect. Deciding that the pathetic dictator is not worth killing, Hakaider turns to leave. Gurjev attempts one final, cowardly attack from behind, but Hakaider sees it coming and kills him in an explosion of white feathers. With Gurjev dead and Jesus Town in ruins, the lone android rides away on his motorcycle into an uncertain future, neither savior nor villain, but an unstoppable force of violent free will.