The Akai clan had branches in Tanba and Kōzuke provinces. Those in Tanba were based in Kuroi Castle in the Hikami District.
In 1526, Hosokawa Takakuni, a kanrei, or deputy shōgun, had Kōzai Motomori executed on the basis of slander from Hosokawa Tadakata.
In 1527, Hatano Tanemichi and his younger brother, Yanagimoto Kataharu, launched a rebellion against Hosokawa Takakuni, a kanrei. Akai Tadaie joined the Hatano clan to raid the forces of Hosokawa Tadakata during a siege of Kataharu at Kannōsan Castle. In the Battle of Katsurakawara, the Hosokawa forces fled in defeat, setting the stage for the fall of Takakuni.
In 1531, Takanuni died in a battle against Akamatsu Harumasa known as the Daimotsu kuzure, whereupon Hosokawa Harumoto from Awa Province succeeded him as kanrei, garnering the loyalty of the kokujin in Tanba. Meanwhile, Hatano Harumichi (Tanemichi’s son), raised arms after pledging support for Hosokawa Harukuni (Takakuni’s younger brother), and the Naitō and Akai clans lost to the Hatano. This battle led to the capture of Kuroi Castle, during which Akai Tokiie and his son, Iekiyo, escaped to the protection of the Bessho clan in Miki in eastern Harima. In 1536, Harukuni took his own life at the Tennō Temple in Settsu, located at an important transit point between Settsu and Izumi provinces. Afterwards, the Akai clan recovered its former territory and Tokiie returned to Tanba Province. Tokiie established a base at Eboshimoyama and clashed with the Naitō.
In 1552, Hosokawa Ujitsuna, the adopted son of Takakuni originating from Hosokawa Tadakata, assembled an army, and with the support of Miyoshi Nagayoshi (a retainer of Hosokawa Harumoto), became a kanrei. After fleeing Kyōto, Harumoto relied upon Hatano Harumichi to enter Tanba. He then received help from Akai Tokiie, setting the stage for confrontation between the Akai clan and Miyoshi Nagayoshi.
In 1553, Naitō Kunisada joined the Miyoshi to assault Yakami Castle, the main base of the Hatano clan in Tanba. This triggered a counterattack by Miyoshi Masakatsu and Kōzai Motonari from behind that led to the capture of Kunisada’s home base of Yagi Castle in Tanba. Kunisada died in the battle, but Matsunaga Nagayori, Kunisada’s son-in-law and a senior retainer of the Miyoshi clan, joined and re-established the Naitō clan, defeated the Hatano, and gained control over nearly all of Tanba Province.
In 1555, the kokujin in the Hikami District were divided between two groups, leading to a conflict at Kōra in the Hikami District of Tanba between the Akai, who supported Hosokawa Harumoto, and the Ashida and Adachi, who supported Hosokawa Ujitsuna. In this battle, Tokiie’s son, Akai Iekiyo suffered serious injuries, while the Ashida and Adachi also lost many men. The Akai gained control over most of the Hikami District. In 1557, Akai Iekiyo died from his earlier injuries. Akai Naomasa then supported Akai Tadaie (Iekiyo’s son), and, in 1565, killed Naitō Munekatsu (formerly Matsunaga Nagayori) at a battle in the village of Waku.
In 1570, the Akai clan surrendered to Oda Nobunaga, bringing calm to their territory. Later, the Akai launched a fierce resistance movement together with a group of kokujin led by the Hatano. Akechi Mitsuhide, a retainer of the Oda, led an invasion into Tanba and captured Kuroi Castle in 1579 at the Battle of Kuroi Castle. Tadaie fled to Futamata in the Toyoda District of Tōtōmi Province.
In 1592, Akai Tadaie served Toyotomi Hideyoshi during the expedition to the Korean Peninsula. In 1593, he received a fief of 1000 koku in the Minō District of Harima. Discord arose between Tadaie and Toyotomi Hidenaga (Hideyoshi’s younger brother), and Tadaie petitioned via Ōkubo Tadayo to serve Tokugawa Ieyasu. He was then ordered to be under Yamaguchi Naoyuki, a relative of the Ashida of Shinano Province. He later served and then left the Toyotomi clan.
In 1600, he participated in the Battle of Sekigahara on behalf of the eastern forces, and after the battle, became a hatamoto with a fief of 2000 koku in Yamato Province.