He was born in Cork on 29 June 1840, as the fifth of five children of John Wheeler Dowden and Alicia Bennett.

In the same year he married, wedding a woman named Louisa Jones, by whom he would eventually father six children.

John continued his studies and received a Bachelor of Divinity (BD) degree from Trinity College.

He is buried with his wife Louisa and son John Wheeler Dowden LLD, FRCSEd (1866–1936), who was president of the Royal College of Surgeons of Edinburgh.

Dowden gave the Rhind lectures in 1901, on "The Constitution, Organisation, and Law of the Mediaeval Church in Scotland".