After the Normans captured Dublin in 1171, a large part of the Norse population left the old city on the south of the Liffey river and settled on the north side, which was known as Oxmantown. Dublin, then, was the capital of the Lordship of Ireland, a nominally all-island state founded by the Normans, and populated by English and Welsh settlers. English rule centered on Dublin Castle, which remained the seat of British rule until 1922. Dublin was also the seat of the Irish parliament, comprised of English members. Important buildings dating back to this time include St Audoen's Church and St Patrick's Cathedral. The last part of the city's medieval walls overlook St Audoen's Church in the direction of Cook Street.

In medieval times, Dublin was a tightly-knit community of 5,000 to 10,000 inhabitants, cultivating certain curious rituals. The mayor of the city, for example, escorted all newlyweds to the bullring, where they would kiss the enclosure for good luck. Outside the city walls were the Liberties, suburbs on the lands of the archbishop of Dublin, and Irishtown, supposedly inhabited by Gaelic Irish who had been expelled from the city under a 15th-century law. Although not officially permitted, native Irish did live in the city, and by the 1500s their language had begun to rival English in everyday life.

In 1348, the Black Plague ravaged the city, as it did most of Europe. There were mass burials in Dublin in the Blackpitts area, a name retained to this day. The last major outbreak of the plague in Dublin was in 1649. The disease recurred regularly over the course of 300 years. To make matters worse, neighboring Irish clans raided the city frequently, and a Scottish army even destroyed the suburbs in 1314.

These factors caused the English to lose interest in maintaining the colony in Ireland, and the Fitzgerald Earls of Kildare took the responsibility to defend the city, dominating Irish politics until the 16th Century. In the unofficial capacity of rulers the Fitzgeralds often pursued their own agenda. During the Wars of the Roses in the late 15th Century, fought between the House of Lancaster and the House of York, they occupied the city and proclaimed a Yorkist king of England. In 1536, the Fitzgeralds, angry that the Earl of Kildare had been imprisoned, besieged the Dublin Castle. King Henry VIII sent troops to restore order and replace the Fitzgeralds with English administrators. Thus Dublin and the Crown began to 'enjoy' a closer relationship.