Kirk is a word of likely Scandinavian origin that is commonly used in Scotland instead of the English "church." With Saint Andrew being the patron saint of Scotland, it is no surprise that the country has many a St Andrew's Kirk. What is notable is that the town of North Berwick has three at least partially still-standing.

The first was originally an eighth-century wooden building near North Berwick's coastline, but the stone construction that remains dates from the 12th century. Following damage to it by a strong storm, a new St Andrew's was built in the Kirk Ports area farther inland. Construction on it lasted from 1658 to 5 June 1664, when its opening was recorded with the notice of “This day the paroch mett in the new kirke for worship.”

St Andrew's at Kirk Ports continued to be the main church in North Berwick, with renovations and extensions taking place for over two centuries. In the 19th century, a population boom caused by growing industry led to its space for 500 churchgoers to become insufficient. The town's second St Andrew's held its last service one year and two days short of the 220th anniversary of its inauguration, on June 3, 1883. The third St Andrew's held its first services just a week later.

The current ruin status of the second kirk was partly by design, as it was decided that upon moving the religious services to the new church, this older one was to have its roof disassembled and the rest of the building stripped of the most valuable materials. The walls would be allowed to stand to become what it is now: a 'picturesque ruin'.