His childhood name is unknown and his common name was Katsuzaburō (勝三郎). His father was Ikeda Tsunetoshi, who served Oda Nobuhide. His mother, Yōtokuin (養徳院), was Oda Nobunaga's wet nurse, and later became Nobuhide's concubine, bearing him a daughter. There are various theories as to his birthplace (including the Owari, Mino, Settsu and Ōmiprovinces). He was one of the four karō at Kiyosu Castle. His official position was Kii-no-kami (紀伊守), or "Governor of Kii Province". His courtesy name was Shōzaburō (勝三郎). He later became a priest and referred to himself as Shōnyū (勝入).
In 1571, Tsuneoki took part in the burning Siege of Mount Hiei to subdue the followers of the Ishiyama-Honganji; attacks against the Nagashima Ikkō-ikki.
In 1573, he participated in the Siege of Makishima Castle against Ashikaga Yoshiaki. Yoshiaki surrendered, and sending Yoshihiro, his eldest son, as a hostage to Nobunaga.
In 1574, he entered the mountain fortress of Ori Castle in eastern Mino to pin-down Akechi Castle after it was taken by Takeda Katsuyori.