The town walls still circuit much of the old settlement, and the market cross at the centre is among the oldest in the country, dating to around the thirteenth or fourteenth century. That so much remains intact in a working town, rather than as a managed ruin in open countryside, gives the place a quality that is quietly disorienting.

The town was founded around 1235 by Meiler de Bermingham, a Norman lord who also established a Dominican friary there in 1241. The friary, dedicated to SS Peter and Paul, became one of the most important in Connacht and its remains are still substantial. The de Birminghams built a castle in the town as well, and the keep survives to a considerable height. Athenry also gave its name to one of the more consequential engagements of the medieval period in the west of Ireland: the Battle of Athenry in 1316, in which the Connacht Irish under Felim O'Connor were decisively defeated by Anglo-Norman forces, a result that shaped the political landscape of the province for generations. The town later went into long decline, which may partly explain why so little of it was demolished or rebuilt in subsequent centuries.