Crail probably dates from at least as far back as the Pictish period, as the place-name includes the Pictish/Brythonic element caer, 'fort', and there is a Dark Age cross-slab preserved in the parish kirk, itself dedicated to the early holy man St. Maelrubha.
Built around a harbour, it has a particular wealth of vernacular buildings from the 17th to early 19th centuries, many restored by the National Trust for Scotland, and is a favourite subject for artists. The most notable building in the town is the 13th century parish church. Though much altered, this is one of Scotland's most beautiful ancient churches, with a fine western tower with small spire, and a double arcade of round pillars of variegated red sandstone in the nave. The side walls were rebuilt in Regency times, and the large pointed windows, filled with panes of clear glass held by astragals rather than leads, allow light to flood into the interior. The unaisled chancel, now housing a huge organ, has been shortened. The church retains some 17th century woodwork, and there is an early Christian cross-slab of unusual form (perhaps 10th century), formerly set in the floor, on display.
The large kirkyard surrounding the building has a fine collection of mural monuments dating from the late 16th century on.
Other historic buildings in Crail include the tollbooth, with a tower dating from about 1600, whch stands on its own in the large marketplace, and the doo'cot (Scots for dovecot) of the town's otherwise vanished Franciscan Friary.
Crail once had a royal castle above the harbour (perhaps this was the site of the 'fort'). The site is still visible as an open garden, but little or nothing of the structure survives above ground. A Victorian 'turret' jutting out from the garden wall recalls the Castle (visible in the photograph reprduced above).
On the beach beside the harbour, there are fossilised trees, dating back to the carboniferous geological period.
Crail Aerodrome, to the north of the town, started life as a naval air station during the First World War. In the runup to the Second World War it became HMS Jackdaw. Planes from the airbase took part in the final attack on the Tirpitz in 1944.
Polish soldiers stationed at Crail during the Second World War helped the Archdiocese of St Andrews and Edinburgh purchase the disused United Presbyterian Church (built 1859). In 1942, it become Most Holy Trinity Church. The Church has recently been renovated and contains an icon to Our Lady of Poland painted by one of the Polish soldiers.
After the war, the airbase was taken over by the Royal Navy and renamed HMS Bruce. Between 1956 and 1958, the airfield was used by the Joint Services School for Linguists to train linguists in Russian.
The airfield site now is home to Crail Raceway. It hosts events every second Sunday of the month, and lets amateur drivers compete with their own adapted vehicles.