Born the son of Ashikaga Yoshiakira, Yoshimitsu became the third shogun at age ten. He grew up guided by Kanrei (deputy shogun) Hosokawa Yoriyuki, and once he began governing directly he worked to strengthen shogunal power. In 1392 he achieved the historic feat of unifying the Northern and Southern Courts, ending some sixty years of divided imperial rule. He actively suppressed the power of the provincial military governors (shugo): he crushed the revolt of Yamana Ujikiyo in the Meitoku Rebellion (1391), eliminated Ouchi Yoshihiro in the Oei Rebellion (1399), and in this way established firm shogunal authority. In 1394 he passed the shogun title to his son Yoshimochi and took Buddhist orders, yet retained real power. He reopened diplomatic relations with Ming China and initiated the Tally Trade (Kangō bōeki), bringing enormous economic and cultural benefit. He built the Kitayama villa (now Rokuon-ji, known as Kinkaku-ji) and patronized Zeami, enabling him to perfect the art of Noh, ushering in the flourishing of Kitayama culture. He died in 1408 at age 51. His pursuit of a status beyond that of shogun — including appointment as Grand Minister of State and the use of the title "King of Japan" — has generated varied assessments in later ages.

He combined superior intelligence and aesthetic sensibility with deep knowledge of culture and the arts, alongside vigorous political ambition. He did not shrink from concentrating power and tended to seek a status that surpassed even the imperial court. His relationship with the Noh master Zeami reveals a sensitive side that deeply understood and supported artists. He possessed a flexible political sense that alternated between diplomatic compromise — as in the unification of the two courts — and a hard line toward the great provincial lords.

Kinkaku-ji (Rokuon-ji) survives as a UNESCO World Heritage Site, known worldwide as the symbol of Kitayama culture. The unification of the Northern and Southern Courts is regarded as one of the greatest political achievements of the Muromachi Shogunate. The Tally Trade promoted economic and cultural exchange between Japan and Ming China and contributed greatly to the development of medieval Japanese culture. His patronage of Zeami also established Noh theatre as a traditional performing art that continues to the present day — a legacy of incalculable importance in the history of Japanese culture.