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Said to be of the Toki clan lineage of Mino Province, though much of his early life remains obscure. After serving Ashikaga Yoshiaki he was taken up by Oda Nobunaga and rose rapidly. He participated in major Nobunaga campaigns including the burning of Mt. Hiei in 1571 and the Battle of Nagashino in 1575, and earned high praise for pacifying Tanba Province in 1579 in preparation for the assault on the Mori clan. By 1582 he had become one of Nobunaga's most trusted lieutenants as the lord faced imminent western campaigns. Yet on 2 June 1582, ordered to march to the western front, Mitsuhide abruptly turned against his master and stormed Honnoji temple in Kyoto, where Nobunaga was lodging. Surrounded, Nobunaga died by his own hand, and the dream of national unification vanished. Mitsuhide moved swiftly to seize Kyoto and Osaka, but a mere thirteen days later he was defeated at the Battle of Yamazaki by Hashiba Hideyoshi, who had raced back from the siege of the Mori. While fleeing, Mitsuhide was caught by peasant hunters and killed in a bamboo grove at Ogurusu at around age 55. The true motive for his rebellion remains disputed and mysterious to this day.

A classic scholar-warrior of high culture and administrative ability, well versed in renga and waka poetry. As lord of Tanba Province he earned the trust of his people through good governance, yet in Nobunaga's proximity he was reportedly under constant strain. The background of his rebellion is thought to involve a complex mix of factors including slights, humiliations, and ideological differences.

The Honnoji Incident is remembered as one of the greatest acts of rebellion in Japanese history, and Mitsuhide's name is permanently engraved as the man who felled the genius Nobunaga. The debate over his motives — the "Honnoji Controversy" — remains a major theme in Japanese historiography to this day, and he has repeatedly been portrayed as the protagonist in NHK historical dramas and novels.