After the death of Masanori AKAMATSU at the master family, Muramune became Shugoshoku (a military officer) of Harima, Bizen, and Mimasaku Provinces with the support of Toshoin, a dowager of Masanori, as well as Uragami clan because Yoshimura AKAMATSU, an adopted son of Masanori AKAMATSU, was still a small child.
主家では赤松政則の死後、その養子である赤松義村が幼年であったこともあり、政則後室である洞松院の後見や、浦上氏などの支持を受ける形で、播磨・備前国・美作国の守護職に就いた。