The Muromachi era (1336-1573) began when the Ashikaga clan established the shogunate in Kyoto.
The castle was supposedly built by Yamana Mochitoyo (1404-1473), the governor of Tajima Province and famous western army general in the Onin War, from 1441 to 1443 during the Kakitsu era.
Takeda Castle played an important role in guarding the border between Harima and Tajima, and also acted as a base for sorties sent to attack Harima.
During the Azuchi-Momoyama era (1568-1600), Toyotomi Hidenaga (1540-1591)—the younger brother of Toyotomi Hideyoshi (1537-1598)—was ordered to attack Takeda Castle. The goal was to subdue the Tajima generals and secure the Ikuno Ginzan silver mine. He succeeded.
The last lord of Takeda Castle was Akamatsu Hirohide (1562-1600), Hideyoshi’s vassal. Hirohide had been part of the Western Army in the Battle of Sekigahara in 1600, but was later invited by the Kamei clan of the Eastern Army to attack Tottori Castle. He attacked the castle, but was blamed for the large fire that broke out there and committed suicide on the orders of Tokugawa Ieyasu (1543-1616).
After losing its lord, Takeda Castle was abandoned in accordance with the policies of the Edo Shogunate established by Tokugawa Ieyasu. It eventually eroded into the ruins we see today where only the stone walls remain.