The settlement began on the north bank of the wide River Great Ouse, perhaps in the fifth or sixth century, at a place where the river could be forded. The Anglo-Saxons called it Slepe - meaning a muddy place, which the riverside marshes amply justified. In 986 the manor of Slepe was bequeathed to Ramsey Abbey, then a newly founded Benedictine house twelve miles north. The abbey needed relics. Saints' bones were the great economic engine of the medieval church - they drew pilgrims, who brought money. In 1001, conveniently, a peasant ploughing a Slepe field turned up a stone coffin containing a complete skeleton. The Abbot Eadnoth declared the bones to be those of St Ivo, a Persian missionary who according to a hastily composed legend had appeared one morning at Slepe carrying a bishop's crozier and announcing his intention to preach the gospel here. Even the editors of the Victorian Dictionary of Christian Biography described the story as utterly improbable - blaming, gently, the monks of Ramsey. But the bones did their work. The town acquired pilgrims, prosperity, and a new name. The seaside town of St Ives in Cornwall, incidentally, takes its name from a different saint - Ia of Cornwall, a holy woman who has no connection at all with this place.

By the time Henry I granted a royal charter for an annual fair in 1110, St Ives had become a major staging point on a drove road that brought cattle and sheep from Scotland and the north of England down to the Smithfield markets in London. The wooden bridge of 1107 was replaced in 1426 by the famous stone bridge, with its rare medieval chapel. The town's weekly cattle market was said to be second only to Smithfield. Drovers needed inns; the town had sixty-four public houses by 1838 - one for every fifty-five inhabitants. The Dolphin has occupied the same site for over three hundred years. The White Hart pre-dates 1720. The Royal Oak's name commemorates Charles II's escape from Cromwell's Roundheads after the Battle of Worcester in 1651. In April 1689 a fire that began in a malt house, driven by a high wind, ran along the Sheep Market, hopped Bridge Street and crossed the bridge itself, consuming much of the town. The market rebuilt. Through the 17th and 18th centuries St Ives stayed a hub for trade, navigation, and the slow business of feeding London.

Between 1631 and 1636 a struggling minor gentleman called Oliver Cromwell lived at Old Slepe Hall in St Ives. He was in his early thirties, recently moved from Huntingdon where he had fallen out with the town's patrons, and farming land he had inherited from an uncle. By all accounts these were lean years - Cromwell would later describe his life at this period as one of religious crisis and material precarity. He read the Bible. He took on local responsibilities. He left in 1636 for Ely, having inherited more land, and seven years after that he was a colonel of cavalry in the Parliamentary army. The St Ives years are not the famous ones. They are the years in which a Cambridgeshire farmer became the man who could organise the New Model Army and overturn a king. A bronze statue of Cromwell by F. W. Pomeroy, erected in 1901, stands today in the market place where he once paid his rent.

The Cambridge and St Ives railway line opened in 1847 and slowly killed the river trade. The town shrank for a while - 3,572 people in 1851, 2,664 by 1931. Then came the post-war expansion. The population reached 7,148 in 1971, 12,331 in 1981, and over 16,000 today. In 1971 a small electronics firm took over the Old Mill - the former flour mill built by Potto Brown in 1854 - and began making the first commercially successful pocket calculators. The firm was Sinclair Radionics, run by Clive Sinclair, who would later create the ZX Spectrum home computer that taught a British generation to code. The mill had previously been a printing works for Chivers jam jar labels. The Norris Museum, founded by a local antiquarian who died in 1931, reopened in 2017 after a £1.5 million refurbishment. The town hosts a free two-day carnival and music festival every summer. The 18-hole golf course sits on the edge. Markets run on Mondays and Fridays, with a farmers' market every other Saturday. The drovers are gone. The man with seven wives, if he ever existed, has not been seen for centuries. The town carries on.