It was founded soon after the Tsaesci abandonment of the town that was later recolonized by the Expeditionary Force, and which would be renamed Septimia. Similar to Septimia, Ionith was an abandoned Tsaesci city that was refounded by the Imperials. The precise date of its founding is unknown, but is estimated to have been built around the beginning of Mid Year, 3E 288.
Three months later, during Hearthfire, civilian ships along with supplies arrived at Septimia, and thus began the brief population and culture of the Akaviri Settlements. Ionith proved to be an important figure in the brief negotiations between the Tsaesci and the Imperials, as both the city negotiations were held in, and the first city attacked after they failed. Ionith's only winter was a harsh one, followed by an even harsher drought in the spring. With their economy weakened, the inhabitants of both Ionith and Septimia underwent a series of attacks, eventually leading to the destruction of Ionith, and the death of Uriel Septim V.