According to the 2006 estimate, the village has a population of 395. Originally, Culross served as a port city on the Firth of Forth and is believed to have been founded by Saint Serf during the 6th century.
The civil parish had a population of 4,348 in 2011.
A legend states that when the British princess (and future saint) Teneu, daughter of the king of Lothian, became pregnant before marriage, her family threw her from a cliff. She survived the fall unharmed, and was soon met by an unmanned boat. She knew she had no home to go to, so she got into the boat; it sailed her across the Firth of Forth to land at Culross where she was cared for by Saint Serf; he became foster-father of her son, Saint Kentigern or Mungo.
During the 16th and 17th centuries, the town was a centre of the coal mining industry. Sir George Bruce of Carnock, who built the splendid 'Palace' of Culross and whose elaborate family monument stands in the north transept of the Abbey church, established a coal mine at Culross in 1575 and in 1595 constructed the Moat Pit by which it became the first coal mine in the world to extend under the sea. The mine worked what is now known as the Upper Hirst coal seam, with ingenious contrivances to drain the constant leakage from above. This mine was considered one of the marvels of the British Isles in the early 17th century, described by one visitor, John Taylor, The Water Poet, as "a wonder ... an unfellowed and unmatchable work", until the Moat Pit was destroyed in a storm on 30 March 1625.
Culross' secondary industry was salt panning.:9-10 There was a considerable export trade by sea in the produce of these industries and the prevalence of red roof tiles in Culross and other villages in Fife is thought to be a direct result of collier ships returning to Culross with Dutch roof tiles as ballast. The town was also known for its monopoly on the manufacture of 'girdles', i.e. flat iron plates for baking over an open fire.
The town's role as a port declined from the 18th century, and by Victorian times it had become something of a 'ghost town'. The harbour was filled in and the sea cut off by the coastal railway line in the second half of the 19th century (though the outer harbour has recently been restored by a local group).
During the 20th century, it became recognised that Culross contained many unique historical buildings and the National Trust for Scotland has been working on their preservation and restoration since the 1930s.
Notable buildings in the burgh include Culross Town House, formerly used as a courthouse and prison, the 16th century Culross Palace, 17th century Study, and the remains of the Cistercian house of Culross Abbey, founded 1217. The tower, transepts and choir of the Abbey Church remain in use as the parish church, while the ruined claustral buildings are cared for by Historic Environment Scotland. Just outside the town is the 18th-century Dunimarle Castle, built by the Erskine family to supersede a medieval castle.
Thomas Cochrane, 10th Earl of Dundonald spent much of his early life in Culross, where his family had an estate. There is now a bust in his honour outside the Culross Town House. He was the first Vice Admiral of Chile.
Several motion pictures have used Culross as a filming location, including Kidnapped (1971), The Little Vampire (2000), A Dying Breed (2007), The 39 Steps (2008), and Captain America: The First Avenger (2011). In September 2013, the Starz television series, Outlander, started filming in Culross for its premiere in August 2014.
The parish of Culross, along with its neighbouring parish of Tulliallan, also Dunblane Diocese, formed a detached part of the earldom, later the stewartry, of Strathearn, which explains why both were in a detached part of Perthshire until 1891, when they became part of Fife.
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