MacCulloch joined the Gay Christian Movement in 1976, serving twice on its committee and briefly as honorary secretary.

He interrupted his teaching to study for the Oxford Diploma in Theology (awarded 1987) at Ripon College Cuddesdon.

In 1987 he was ordained a deacon in the Church of England and from 1987 to 1988 he served as a non-stipendiary minister at All Saints' Clifton with St John's in the Diocese of Bristol.

However, in response to a motion put before the General Synod in 1987 by Tony Higton regarding the sexuality of clergy, he declined ordination to the priesthood and ceased to minister at Clifton.

[citation needed] In 1996 his book Thomas Cranmer: A Life won the James Tait Black Memorial Prize.

[5] In 2011, he delivered the Gifford Lectures on Silence in Christian History: the witness of Holmes' Dog at the University of Edinburgh.

[11] In addition to his position at St Cross College, he has been a senior research fellow in church history and archivist at Campion Hall, Oxford since 2020.

[15][16] In 2021, he was awarded a Festschrift titled "Contesting Orthodoxies in the History of Christianity: Essays in Honour of Diarmaid MacCulloch".