Originating from Harima Province, the Akamatsu clan reached its peak during the early Sengoku period. Akamatsu Masanori served as the ninth lineal head of the clan and sengoku daimyō of Harima, Mimasaka, Bizen and one-half of Kaga province. Several months before his unexpected death from illness in 1496, the Imperial Court conferred upon Masanori the title of Junior Third Rank. Masanori was succeeded by Akamatsu Yoshimura. Yoshimura, however, was still young, so the Uragami and Bessho clans, both shugodai, or deputy military governors, rose in influence while the position of the Akamatsu began to wane.
As Yoshimura matured, he took control of the administrative functions and implemented policies in an effort to bolster his role as a daimyō. Discord then arose between Yoshimura and Uragami Muramune, leading to a struggle from 1518. Muramune prevailed, and, under pressure from Muramune, Yoshimura ceded his power to Akamatsu Harumasa. Yoshimura was assassinated upon orders of Muramune in 1521. Harumasa served as a puppet of Muramune, while the Akamatsu family fell into decline.
Muramune wielded power for the ensuing decade, until chaos erupted after the Uragami clashed with opponents in Harima. In 1531, Harumasa killed Muramune in a battle known as the Daimotsu kuzure, or the Collapse in Daimotsu. This temporarily raised Harumasa’s stature as a daimyō, but resistance from elements of the Uragami clan remained within the Akamatsu territory, and the area under direct control by the Akamatsu family was limited to the western portion of Harima. The head of the Akamatsu no longer had authority over the deputy military governors at the provincial or district level.
In 1537, Amago Haruhisa from Izumo Province, a sengoku daimyō, commenced an attack that led Harumasa to flee to Awaji Province. A majority of the retainers switched loyalty to the Amago, leaving only Bessho Nariharu, a deputy military governor from eastern Harima, to continue the resistance with Harumasa. With additional support from the bakufu, and after fierce fighting, Harumasa succeeded in driving the Amago forces from Harima.
In 1552, Amago Haruhisa was appointed military governor of Bizen and Mimasaka provinces, resulting in a loss by Harumasa of control over these territories.
In 1554, Miyoshi Nagayoshi, a sengoku daimyō from Settsu province, invaded eastern Harima. The Bessho clan attempted to resist, but almost the entire eastern portion of Harima fell to the Miyoshi.
In 1558, Harumasa lost an internal struggle for control with his son, Yoshisuke, and he came under the protection of Akamatsu Masahide, his son-in-law. While continuing to oppose Yoshisuke, Harumasa joined with Masahide to dominate western Harima. At this time, he approached Mōri Motonari, who was greatly expanding his influence in the western region of the country with the aim of reviving his governance, but failed to complete the task.