The name "Kingcase" has been traditionally associated with William Wallace and King Robert Bruce, both great Scottish Heros. A suggestion that a chapel was founded here by missionaries from Whithorn would, if true, make it one of the earliest religious sites in Scotland. In the middle ages there was a hospital at Kingcase which catered, amongst others, for leprosy, at that time the term was used of almost any skin disease

The later history of an establishment at Kingcase as a place of worship was as a mission hall under the direction of St Cuthberts Parish Church, later transferred to the modern St Nicholas' at it's inception in 1908.

The history of the modern church begins immediately after the Union of the Churches in 1929 which brought the four churches in Prestwick together within the Church of Scotland. A new congregation was formed in what was the New Prestwick mission hall of of St Nicholas Church. This congregation was recognised as Prestwick Kingcase Church in 1934 becoming a parish church in 1950

The main part of the existing church building was constructed in rectangular form, with the pulpit at the north end, just before the first world war and was extended in 1955-56 by the addition of the chancel and two transepts and the resiting of the pulpit at the south end of the building.

Various additions in the form of halls were constructed culminating in the purchase of the adjacent Observer Corps property which had become vacant due to the "Standing Down" of that unit. The main building of that complex "The Bunker" has since been demolished and the space given up to car parking

The congregation of Kingcase has risen over the years from 164 in 1935 to 1220 in 2001. Much of this can be ascribed to new housing in the area and a rising population.