Said to be from Izumo Province and reportedly a shrine maiden of Izumo Grand Shrine. Both her birth and death years are unknown, but she is generally thought to have been born around 1572. Around 1603 she founded her own "kabuki dance" at Shijo Kawara in Kyoto, drawing on the popular念仏 (nembutsu) dances of the day, and attracted great audiences. Her reputation spread from the novelty of cross-dressing to play the opposite sex and bold incorporation of contemporary fashions. She performed at Kitano Tenmangu shrine and Edo Castle, and her fame spread nationwide. She is said to have toured various provinces with her partner Saruwaka (also known as Nagoya Sanzaburo). Almost no records survive of the rest of her life; some accounts say she returned to Izumo in old age and became a nun, while others say she died young, but neither has been confirmed. Her dances evolved through later yūjo (courtesan) kabuki and wakashu (youth) kabuki into the kabuki of today.

Free-spirited and richly creative, she had a keen sensitivity to the mood of the times. Unbound by existing conventions, she boldly crossed gender boundaries in her performances. Her charismatic stage presence, which captivated audiences, combined with her innovative artistic spirit, elevated her dancing into a historical event.

As the person who created the direct origins of present-day kabuki, she is one of the most important figures in the history of Japanese performing arts. The "kabuki dance" she created evolved into kabuki as a mature classical art form, which is now registered as a UNESCO Intangible Cultural Heritage. A statue of Okuni stands by the Shijo Bridge in Kyoto, conveying her achievement to the present day.