When Takakuni HOSOKAWA and Harumoto HOSOKAWA fought for the position of Kanrei, Naganao participated in the war together with his elder brother, Yojuro Naganobu as a member of the Harumoto side and, after the victory of Harumoto, he served as a close aide of Harumoto because his brother assumed the position of Yamashiro Gundai (Intendant of a region or administrator of a town) to supervise the territory of Hosokawa family in Yamashiro Province.
細川高国と細川晴元が管領の地位を巡って争った際には、長直は兄である与十郎長信とともに晴元側の一員として参戦し、晴元の勝利後には兄が山城郡代として山城国内の細川領を監督する地位に立ったために、長直も晴元の近臣として仕えた。