After defeating Akechi Mitsuhide at the Battle of Yamazaki, Toyotomi Hideyoshi (then known as Hashiba Hideyoshi) sent his forces to Sakamoto Castle, Mitsuhide's stronghold. Cornered, retainer Akechi Mitsuharu and Mitsuhide's wife and children took their own lives, and the castle burned down — completing Hideyoshi's suppression of Mitsuhide.

In 1571, Oda Nobunaga ordered his retainer Akechi Mitsuhide to build a castle at Sakamoto, at the foot of Mt. Hiei on the shore of Lake Biwa. Built at a strategic point linking Otsu and Kyoto, this water castle became Mitsuhide's stronghold for governing Omi Province and supported Nobunaga's campaign to unify Japan.

In 1571, Akechi Mitsuhide was granted Omi Province by Oda Nobunaga in reward for his role in the burning of Mount Hiei, and built Sakamoto Castle on the shore of Lake Biwa as his residence. After killing Nobunaga in the Honnoji Incident of 1582, Mitsuhide was defeated and killed at the Battle of Yamazaki; shortly after, as Hideyoshi's forces closed in on Sakamoto, senior retainer Akechi Hidemitsu and Mitsuhide's wife and children took their own lives, and the castle burned to the ground.