Aire-la-Ville was first part of the domain of the Count of Geneva, then of the House of Savoy.
It was a Bernese bailiwick from 1536 to 1567, and in 1589 the Genevans took the nearby Castle of Ternier.
After the Treaty of Lyon in 1601, it became French, then part of the Kingdom of Piedmont-Sardinia in 1760.
Following the annexation of Savoy by France in 1792, it was ceded to Geneva in 1816 and joined the Swiss Confederation.