Awaya Motohide served as a bushō and retainer of the Mōri clan. Motohide, and his grandson, Awaya Motochika, were included in the notable Eighteen Generals of the Mōri.
In 1490, Mōri Hiromoto granted Motohide income of one-hundred and fifty kan mon from Toyoshima in Aki Province. Motohide accompanied Mōri Okimoto in a deployment for Ōuchi Yoshioki. Beginning in 1507, he was stationed in Kyōto for a period of four years. In 1509, Okimoto assigned to Motohide additional income from certain families in the village of Tsuda in Bizen Province. In 1517, he made contributions at the Battle of Arita-nakai as a member of the allied Mōri and Kikkawa forces against the Takeda clan of Aki, serving as the first battle for Mōri Motonari. Afterwards, Motonari relied heavily on Motohide.
In 1523, Mōri Kōmatsumaru died prematurely, triggering a struggle for succession in the Mōri clan between Motonari and Aiō Mototsuna. Around this time, Motohide received instructions from Awaya Motokuni (the head of the Awaya clan) and Shiji Hiroyoshi (the administrator for the Mōri) to visit Kyōto under the pretext of visiting shrines and temples with the actual intent of appealing to the shōgun. After garnering the support of Ashikaga Yoshiharu, the twelfth lineal shōgun, Motonari’s supporters succeeded making him the successor as head of the clan. Motohide’s seal is included among fifteen elder retainers of the Mōri who published a joint declaration of support. Later that year, Motonari allocated territory in the Saijō area of Aki to Motohide. In 1529, Motohide contributed at the Battle of Matsuo in Aki and received a letter of commendation from Motonari.