Macquarrie was born in Renfrew, Scotland (on the River Clyde, approximately six miles from Glasgow) into a devout Presbyterian family (his father was an elder in the Presbyterian Church of Scotland) with strong Gaelic roots.

Educated at Paisley Grammar School, he read philosophy at the University of Glasgow under the distinguished scholar Charles Arthur Campbell (M.A. 1940) and obtained a degree in theology (B.D. 1943).

He enlisted in the British Army and served from 1943-48. Ordained in 1945, he served in the Royal Army Chaplains Department 1945-48.

After demobilization he served as a parish minister in the Church of Scotland at St Ninian's Church, Brechin (1948-53).

He died on 28 May 2007 at the age of 87. His widow Jenny died in August 2008. He is survived by two sons and a daughter.

The archives of John Macquarrie are maintained by the Bodleian Library, Oxford.

Macquarrie returned to the University of Glasgow to study for a Ph.D., which he was awarded in 1954 while serving as lecturer in systematic theology at Trinity College, Glasgow. His supervisor was Ian Henderson who, despite having been a pupil of Karl Barth at Basle, was theologically more closely aligned with his disputant Rudolf Bultmann.

In 1962 Macquarrie was appointed Professor of Systematic Theology at Union Theological Seminary, New York City. During his time in the United States Macquarrie became a member of the Anglican Communion. He had long been attracted to the Anglican Church but in deference to his family's feelings and their strong Presbyterian roots maintained his worship in the Church of Scotland. He was later ordained deacon and priest in the Episcopal Church in the United States of America. He was ordained priest by the Bishop of New York on 16 June 1965 and the next day (the Feast of Corpus Christi) he celebrated his first Eucharist at the Church of St Mary the Virgin in New York City.

He was Lady Margaret Professor of Divinity in the University of Oxford and Canon Residentiary of Christ Church, Oxford from 1970 until 1986. On retirement he continued to live in Oxford and was appointed Professor Emeritus and Canon Emeritus. From 1996 he had been the Martin Heidegger Professor of Philosophical Theology at the Graduate Theological Foundation in the United States.

Macquarrie was awarded the Territorial Decoration in 1962. In 1964 the University of Glasgow conferred the degree of Doctor of Letters on him and in 1969 the university awarded him the degree of Doctor of Divinity honoris causa. On his appointment to the Lady Margaret chair at Oxford he incepted as a Master of Arts. In 1981 he became a Doctor of Divinity of the University of Oxford and in 1984 he was elected a Fellow of the British Academy. He has also received the honorary degrees of Doctor of Sacred Theology from the University of the South (1967) and the General Theological Seminary (1968), Doctor of Divinity from the Episcopal Theological Seminary of the Southwest (1981), the University of Dayton (1994), and the Graduate Theological Foundation, Indiana, and Doctor of Canon Law from Nashotah House (1986).

He was the Gifford Lecturer for 1983-84, lecturing on the topic In Search of Deity.

Macquarrie can be safely categorised as both an existentialist and a systematic theologian. His most important philosophical influence is the work of Martin Heidegger. Macquarrie remains one of the most important commentators and explainers of Heidegger's work. His co-translation of Being and Time into English is considered the canonical version. Macquarrie is also perhaps the most important English-language expositor on the theological and philosophical work of Rudolf Bultmann.

Among Macquarrie's most widely read books are his Existentialism, meant as an introduction to the subject, and what is perhaps his masterpiece: Principles of Christian Theology, a work of systematic theology that aims both to harmonise existentialism and orthodox Christian thought and to offer a highly-intellectualised apology of the Christian faith. Macquarrie's work is characterised by a remarkable even handedness to all sides and viewpoints and, although not readily accessible to those without a good background in philosophy, his writing is considered engaging and often witty - at least judged by the standards of existentialism and systematic theology.

Macquarrie believed that truth value could reside in other faith traditions, although he rejected syncretism. In his book Mediators Between Human and Divine: From Moses to Muhammad (1996), he wrote:

In 1964 I published an article entitled 'Christianity and Other Faiths'... [and] I continue to hold the views I expressed then... I believe that, however difficult it may be, we should hold to our own traditions and yet respect and even learn from the traditions of others. I drew the conclusion that there should be an end to proselytizing but that equally there should be no syncretism of the kind typified by the Baha'i movement. (p. 2)

In that book, Macquarrie commented on what he called 9 historical figures who were viewed by their followers as mediators between the human and the divine (however it was conceived), Moses, Zoroaster, Lao-Tzu, Buddha, Confucius, Socrates, Krishna, Jesus, and Muhammad. Regarding these "mediators," Macquarrie wrote that

[T]here will be no attempt to show that any one of [the mediators] is superior to the others... what has already been said... has shown the impossibility of any such judgment. No human being - and certainly not the present writer - has the exhaustive knowledge of the several mediators or the requisite criteria for making such a judgment. Neither does he or she have the detached situation that would enable a purely objective view of the question. Only God, I suppose, could make such a judgment. (p. 12)

He concluded that

I do not deny for a moment that the truth of God has reached others through other channels - indeed, I hope and pray that it has. So while I have a special attachment to one mediator, I have respect for them all and have tried to give a fair presentation of each. (p. 12)