Given a list of familiar virtues, tolerance is unlikely to be the one most readily associated with Christianity. And with good reason: one does not have to be an expert in church history to know that Christians have a fantastically good record of falling out with one another, with other monotheists, and with nonbelievers, and then finding some excuse to oppress, persecute or kill those who fall on the wrong side of the line.

This is not to say that the secular history of the west, which zigzags its way from the Crusades, through the Inquisition and the Thirty Years' war, to British imperial exploitation is the correct one. Instead it is to recognise that there is much within the logic and language of Christianity to justify intolerance. If eternal salvation/damnation is at stake, what does a little temporal coercion matter? "Compel them to come in," as St Augustine quoted, fatefully, with reference to the schismatic Donatists.

Yet, if the Bible carried with it the logic of intolerance, it also bore the logic and language of tolerance. This came in the concept of adiaphora – "things indifferent" – derived primarily from Paul's first letter to the Corinthians and referring to the conviction that some matters, such as eating meat sacrificed to idols, were not essential to faith.

The idea bore fruit, albeit painfully slowly, in the 16th century, when (some) reformers began to argue that the magistrates' power (which they had recently boosted considerably) should be limited – not only by the imperative not to legislate against God's law (an imperative that was universally acknowledged) but also the imperative not to "command certain indifferent things as if they must be done of necessity". Thus Robert Barnes, an early English reformer (and martyr) argued that there were a number of activities that God apparently neither prescribed nor proscribed, and that "an erroneous situation" would be created "by enacting them into laws".

It was from this idea that the concept of toleration arose. At first, and not surprisingly, it was advocated most insistently by those who were on the religious periphery and thus had most to gain from it. Some puritans liked to cite, for example, the story told in Luke 9, when Jesus rebuked those disciples who had wanted to call down fire on a Samaritan village, in order to show how Christ had commended love even for those of a different creed.

Although it was only the more daring "dissenters" who argued along these lines in the early 1600s, by the end of the century it was the well-connected and well-respected Anglican philosopher John Locke who was making the most cogent case for toleration.

Locke had initially been opposed to religious tolerance but experiences abroad and a careful reading of the gospels persuaded him that "toleration [is] the chief characteristic mark of the true Church". From the (questionable) observation that "scripture speaks very little of polities anywhere … and God doth nowhere by distinct and particular prescriptions set down rules of governments and bounds to the magistrate's authority", Locke was able to draw a crucial distinction between sin and crime, between religious transgressions and political ones. The church had its rightful sphere (of spiritual government) and the state its (of temporal government), and short of some gross incursion from one or the other, an incursion that the civilised Locke found it hard to imagine, the two spheres could coexist happily.

Many years later we can see that Locke's scheme was overly neat and simplistic, to the point of being basically wrong. But coming when it did, after 150 years of religious conflict, it was a bold, brilliantly argued and much-needed justification of toleration.

Christianity helped find a way through the toleration maze in the 16th and 17th centuries by drawing on and working through biblically grounded ideas of what was and wasn't indifferent to temporal affairs. It is only fair to recognise that Christianity had, in fact, constructed much of that toleration maze in the first place, but that does not change the fact that the modern, western commitment to political and religious toleration owes a huge amount to the Bible.

This article first appeared in the Guardian.