The castle was built by one of Connacht's most notable Gaelic lordly families the Ó Flaithbheartaigh clan (the name later anglicised to O'Flaherty).

By this time the O'Flahertys controlled most of Iar Connacht, a territory comprising some 250,000 acres and affording extensive access to the Atlantic seaboard, and trade with Europe.

Aughnanure kept Galway supplied during the Cromwellian siege of 1652; when the castle was controlled by the Earl of Clanrickard, and abandoned when the city surrendered.

He donated it to the State in 1952, recognising that its archeological, historical, and architectural significance would be best preserved that way; however, shortly after completing his gift, he died.

It is now managed by the Office of Public Works, the Irish State body responsible for national monuments and historic properties.