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A companion of Miyoshi Chokei, he was a retainer of Miyoshi Masanaga from the 1540s. He directed the conquest of the province of Yamato in the 1560s and by 1564 had built a sufficient power-base to be effectively independent. It is believed that he was conspiring against Chokei during this period, from 1561 to 1563 three of Chokei's brothers and his son Yoshioki died. This left Miyoshi Yoshitsugu the adopted heir when Chokei died in 1564, too young to rule. Three men shared his guardianship - Miyoshi Nagayuki, Miyoshi Masayasu, and Iwanari Tomomichi.
In 1565, the guardians and Hisahide worked together and dispatched an army to capture Ashikaga Yoshiteru, the shogun, who was then either murdered or forced to commit suicide. His brother Ashikaga Yoshiaki fled and the shogun was replaced by his young cousin, Yoshihide.
In 1566, fighting started between Hisahide and the Miyoshi. Initially the forces of Hisahide were unsuccessful and his apparent destruction of the Buddhist Tōdai-ji in Nara was considered an act of infamy.
In 1568 Oda Nobunaga, with the figurehead Yoshiaki, attacked Hisahide. Nobunaga captured Kyoto in November and Hisahide was forced to surrender. Yoshiaki was made shogun, a post he held only until 1573 when he attempted to remove himself from Nobunaga's power. Hisahide kept control of the Yamato and served Nobunaga in his extended campaigns against the Miyoshi and others, for a while. In 1573 Hisahide briefly allied with the Miyoshi, but when the hope for successes were not achieved he returned to Nobunaga to fight the Miyoshi. In 1577 he split with Nobunaga again, this time Nobunaga turned on him and besieged him at Shigisan Castle. Defeated but defiant Hisahide committed suicide, he ordered his head destroyed to prevent it becoming a trophy (in which his son, Matsunaga Kojiro grabbed Hisahide's head and jumped off the castle wall with his sword through his throat) and also destroyed a priceless tea kettle (Hiragumo) that Nobunaga coveted before he died. His son, Hisamichi, also committed suicide in siege.
Hisahide often appears as a shriveled and scheming old man in fiction. However, this is a fictitious image propagated in response to the assassinations and the destruction of Tōdai-ji that he was believed to have perpetrated. In truth, he was a tall, handsome, and educated man as well as a patron of arts.
In Sengoku Basara series and anime,he is shown as an opportunistic warlord,only striking when his enemy is distracted by problems.In anime,he doesn't care what happens around him.His only sights are for unique and rare items and looted them in any means necessary.