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Born second son of Ashikaga Sadauji in Shimotsuke Province, Takauji grew up as a powerful vassal of the Kamakura Shogunate. When Emperor Go-Daigo launched his movement to overthrow the shogunate (the Genko Incident, 1331), Takauji initially responded on the shogunate's behalf, but in 1333 he captured the Rokuhara Tandai and switched sides, helping establish the Kenmu Restoration. However, he attracted the support of warriors dissatisfied with the aristocratic politics centred on the emperor, and in 1335 used the Nakasendai Rebellion as a pretext to break with Go-Daigo. Though he was forced to retreat to Kyushu, he rallied at the Battle of Tatarahama, retook Kyoto, and in 1336 promulgated the Kenmu Shikimoku as the basic principles of warrior government, enthroning Emperor Komyo and inaugurating the Northern Court. Appointed Seii Taishogun in 1338, he opened the Muromachi Shogunate, but the political situation remained exceedingly complex — torn by conflict with his brother Tadayoshi (the Kannō Disturbance) and the split between Northern and Southern Courts. He remained the central figure in the turmoil of the Northern and Southern Courts until his death at 54 in 1358. Though his rule never fully stabilised, he laid the groundwork for the roughly 240-year Muromachi shogunal system.

A complex personality combining vigorous warrior temperament with sensitive emotionality. On the battlefield he displayed fearless bravery, while tradition holds that he at times sank into deep melancholy. He exhibited many contradictions and inner conflicts in his personal relationships — his complex mixture of love and hatred toward his brother Tadayoshi, his ambivalent feelings toward Emperor Go-Daigo. His charismatic magnetism drew many warriors to him, but he lacked political consistency.

As founder of the Muromachi Shogunate he laid the foundation of a samurai government that lasted some 240 years. His political achievement in establishing the shogunal system despite the turmoil of the North-South Court split was considerable. At the same time he was long regarded as a "traitor" to Emperor Go-Daigo — a judgment that persisted until the Meiji Restoration — and his historical reputation suffered accordingly. Today he is reassessed as a ruler who stabilised the shogunate within the complex political circumstances of the Northern and Southern Courts period. Shrines and temples associated with Takauji remain in Tokyo, Kamakura, and other locations.