The area of present day Akiruno was part of ancient Musashi Province. The in post-Meiji Restoration cadastral reform of July 22, 1878, the area became part of NIshitama District in Kanagawa Prefecture. The town of Itsukaichi was created on April 1, 1889 with the establishment of municipalities law. Nishitama District was transferred to the administrative control of Tokyo Metropolis on April 1, 1893. Itsukaichi expanded through annexation of neighboring villages in 1918 and 1955. Higashiakiru, Nishiakiru, and Tasai grouped together on April 1, 1955 to form the town of Akigawa, which was elevated to city status on May 5, 1971. The city of Akiruno was created on September 1, 1995 by the merger of the city of Akigawa with the neighboring town of Itsukaichi.