Built in 1210 as a royal fortress, the castle was constructed on the orders of King John of England to control this vital crossing point between Leinster and Connacht. The site may have held earlier fortifications, but it was John de Grey, Bishop of Norwich and Justiciar of Ireland, who began building the stone castle we see remnants of today. The construction wasn't without incident; in 1211, a stone tower collapsed, killing Richard de Tuite and eight others, possibly because the builders had attempted to place a heavy stone keep atop a motte that hadn't properly settled.

The castle's early years were marked by complex land dealings and compensation claims. Built on monastic lands belonging to the nearby priory of Saints Peter and Paul, the Crown had to negotiate various exchanges with the Prior of Athlone, including annual payments and land swaps. Geoffrey de Constentin, who had originally been granted the lands in 1200, was given alternative territories in Connacht when the castle became royal demesne. Throughout the thirteenth century, substantial sums were spent on fortifications and repairs; between 1276 and 1279 alone, over £5,000 went towards work at Athlone, Rindown, and Roscommon castles. Much of the surviving medieval fabric, including the river wall with its distinctive three-quarter-round towers at each corner, likely dates from these extensive building campaigns.

The castle's strategic importance meant it frequently changed hands during medieval conflicts. In 1315, Ruaidri O Conchobhar burned the town, though the castle itself may have held out. By the late medieval period, Irish families often controlled the fortress until the Crown finally recovered it in 1537. From 1569 onwards, it served as the residence of the Presidents of Connacht, cementing its role as a symbol of English authority in the west of Ireland. The castle continued to be maintained and modified well into the modern period, with repairs recorded as late as 1547 when William Brabazon, the King's Treasurer in Ireland, oversaw renovations despite local Irish opposition.