The church was erected by Lady Willoughby de Broke in memory of her husband. She laid the foundation stone on 24 July 1856 and the new church designed by John Gibson (architect) was consecrated by the Bishop of St. Asaph on 23 August 1860 after construction at a cost of £60,000. The new parish of Bodelwyddan was created on 3 August 1860, from the communities of Bodelwyddan, Faenol and Pengwern, which until that date had been part of the parish of St. Asaph.
The church contains pillars made of Belgian Red marble, and the nave entrance is made from Anglesey marble. It also contains elaborate woodwork and stained glass, and is a popular tourist destination.
Immediately to the west of the church is Kinmel Park, which was a military camp used by Canadian troops during the First World War. The churchyard contains the graves of numerous victims of the Spanish flu pandemic of 1918-19 in the camp. On 4-5th March 1919 a riot occurred in the camp when the ship allocated to return the troops to Canada was diverted to carry food supplies to Russia, and five Canadian soldiers were killed in the disturbances and subsequently buried in St Margaret’s Churchyard; a common story is that they were executed for mutiny, but this has been denied by the Canadian Department of National Defence.