Born on 5 December 1537, the son of the shogun Ashikaga Yoshiharu, the twelfth of that name, and Keiju-in, daughter of Konoe Hisamichi, destined for monastic life as a younger son of the Ashikaga shogunate, he entered the Kofuku-ji temple, before returning to secular life and taking the name Yoshiaki when his elder brother, the shogun Ashikaga Yoshiteru, was assassinated by the Miyoshi clan in 1565. He came of age on 15 April 1568, formalising his change of name.

After several years wandering in search of a protector powerful enough to restore him to Kyoto, he found the decisive ally in Oda Nobunaga: Oda’s armies entered Kyoto in 1568 and re-established the Muromachi shogunate, with Yoshiaki becoming the fifteenth and last Ashikaga shogun, though reduced to a figurehead; his Nijo residence, a symbol of his authority, was built in 1569. Yoshiaki grew resentful and, from 1570, secretly organised a broad anti-Nobunaga network of alliances bringing together the Takeda, Asakura and Azai clans as well as the Ikko-ikki Buddhist leagues, even seeking help from Takeda Shingen, who died before reaching Kyoto.

Discovered and defeated, he was driven out of Kyoto in 1573, effectively ending the Ashikaga shogunate after more than two centuries; Nobunaga spared his life but banished him, and Yoshiaki became a Buddhist monk under a monastic name. Taking refuge from 1576 at Tomo, in present-day Fukuyama, where historians place a “Tomo Shogunate,” he continued resisting Nobunaga and then his successor Toyotomi Hideyoshi until around 1590, before formally renouncing his title in 1588 under the protection of Hideyoshi, whose pensioned client he remained until his death on 19 October 1597, aged fifty-nine.