Yoshimi was the abbot of a Jōdo monastery when he was first approached in 1464 by Hosokawa Katsumoto, who wished to support a bid for Yoshimi to become shogun. He originally sought to stick to his religious life, and had no desires to become shogun. However, by 1464, he was convinced to join his brother, the shogun, and assist him, putting himself into a position to be the next in the line of succession. The birth of the Shogun's son placed Yoshimi in an awkward situation, making his succession no longer definite, but he remained as Yoshimasa's Deputy.
Despite Yoshimi's support by Hosokawa, it was Hosokawa's opponent, Yamana Sōzen, who stayed in Yoshimi's mansion for a time, and who attended a ceremony in March 1467 honoring the shogun and his brother. Hosokawa did not attend, as he was preparing for the imminent war between himself and Yamana, who supported the succession of the shogun's infant son Ashikaga Yoshihisa.
Following the initial battles between Hosokawa and Yamana within the capital (Kyoto), the Ōnin War turned into a war between Yoshimi and his brother the Shogun. Through a set of complicated events, Yoshimi became one of Yamana's chief generals, and was declared a "rebel" by the Emperor, and stripped of his court rank. That same year, 1469, the shogun officially named his son heir.
Yamana and Hosokawa both died soon afterwards, in 1473, and the Ōnin War came to an end in 1477, along with Yoshimi's political aspirations.