The site on which the parish church is built appears to have religious associations that pre-date the parish church's foundation in early mediaeval times, as evidenced by an 8th-century cross-slab preserved in the church.[1] The parish church was itself dedicated (in the 13th-century) to the early holy man St. Maelrubha of Applecross in Wester Ross.

Crail Castle was an occasional residence of David I of Scotland during the 12th century but subsequently fell into ruin.[2][1]

Crail became a royal burgh in 1178 during the reign of King William the Lion.[3] Robert the Bruce granted permission to hold markets on a Sunday.[1]

Mary of Guise, afterwards consort of James V, landed in Crail in June 1538 after a severe storm, and was hospitably entertained in the ancient mansion of Balcomie Castle, whence, accompanied by the king, she proceeded to St. Andrew's.[4]

John Knox, visiting Crail on his way to St Andrews in 1559, was moved to deliver a sermon in Crail Parish Church. Afterwards, protesters went through the church and forcefully removed images which were put in place by previous generations but were now considered ideologically unsound.[5] In August 1583, many of the inhabitants of Crail attacked nearby Wormiston House, which belonged to Sir John Anstruther. They filled up newly made ponds and ditches, and destroyed a plantation of ash trees. They were vexed at Anstruther because his new ditches had been built on land they claimed to belong to them as common land. The Privy Council of Scotland ordered them to rebuild the dykes.[6]

In 2017, the Community Council was granted the Letters Patent to the Crail Shield and Coat of Arms.[7] This was lost when the Royal Burgh of Crail Council was abolished in 1976.