People have lived around Bridlington since the Bronze Age. The 2.5-mile Danes Dyke at Flamborough Head dates from then. A Roman road from York, now called Woldgate, runs east across the Wolds and into the town. Coin hoards have surfaced near the harbour, and two Greek coins from the second century BC suggest the port was already busy before the Roman conquest. In the fourth century, Count Theodosius set up signal stations along this coast to warn of Saxon raids, and Bridlington Bay may have been the Roman maritime station the ancients called Gabrantovicorum. The modern name comes from later Anglo-Saxon settlers. Bretel, or Bridla, or Berhtel had a farm here, and that personal name was attached to the Old English -ingtun, a small farming community. The Domesday Book records it as Bretlinton, the meeting place of the Hunthow Wapentake.

Walter de Gant founded the Augustinian Priory in 1113, one of the earliest in England. The town that grew around it stayed inland, half a mile from the sea, clustered around the church and the wapentake meeting. The harbour developed separately down at the shore. When the priory was dissolved under Henry VIII, the last prior was hanged at Tyburn and the stone went to build the harbour piers. King John gave Bridlington a weekly market in 1200 and Henry VI added three annual fairs in 1446, two of them on feast days of John of Bridlington, the local saint canonised in 1401. The town divided into Old Town up the hill around the priory and the harbour quarter down at the water, and that division still shapes the street pattern.

Bridlington Spa opened in 1896 and the resort hit its peak in the years that followed. Wallace Hartley, the violinist who would lead the orchestra on the Titanic as the ship went down on 15 April 1912, conducted music in Bridlington in 1902. A blue plaque marks that connection. Composer and conductor Herman Darewski directed light music at the Spa from 1924 to 1939 and has his own plaque in the town. The Royal Air Force kept training schools here in the Second World War, collectively called RAF Bridlington. Air raids hit the town and killed civilians. The 1104 Marine Craft Unit stayed operational until 1980, long after the holidaymakers had started to drift away to package tours abroad.

What kept Bridlington going as the seaside trade declined was the harbour. The lobster boats and the shellfish economy now drive the working town, with retail and summer tourism alongside. The RNLI station on South Marine Drive has stood since 1805, manned entirely by volunteers, and took delivery of a Shannon-class lifeboat in 2018. In 2013 David Hinde, the first Bridlington town crier since 1901, gave a special proclamation outside the priory ahead of a visit by Prince Charles and Camilla for the priory's nine-hundredth anniversary. He recorded his cry at 114.8 decibels at Sewerby Park that August and went on to play the Walmington-on-Sea town crier in the 2016 Dad's Army film. Jake Thackray once mocked the town in song. Bridlington has not seemed to mind.