Oguni Akimoto was the heir of Kurazo Awa no Kami, a retainer of the Mogami clan. In 1580, after Mogami Yoshiaki destroyed the Tendo clan, Yoshiaki crossed the Yamanato Pass to invade the Oguni district, territory of the Mogami-Hosokawa family, defeating Hosokawa Naomoto at the Battle of Mankigahara. Awa no Kami distinguished himself in this battle and was granted the Oguni district by Yoshiaki. His son, taking the surname Oguni, rebuilt the former Mogami-Hosokawa residence at Iwabe-date into Oguni Castle and made it his seat. In 1622, when the Mogami clan was dispossessed (the Mogami Disturbance), Akimoto and the Oguni family were placed in the custody of the Nabeshima of Saga Domain and left the Oguni district, at which point the castle was abandoned.

A practical local lord who inherited his father's military achievements and consolidated his rule by building a castle on his newly granted domain.

Oguni Castle served as the administrative base for Mogami rule over the Oguni district, but was abandoned when the Mogami clan was dispossessed; its remains survive today as a historic site.