The importance of the town owes much to its position at the crossing of the River Ouse by Ermine Street. Traces of a Saxon settlement have been found from the seventh century, and in the tenth century the Danes constructed defensive earthworks here. Evidence that a market was held here, and the existence of a mint at least from the reign of Eadwig (955-959) both testify to the early importance of Huntingdon as the shire town.
William the Conqueror is said to have visited Huntingdon in 1068, and ordered a castle to be built. Domesday Book (1086) states that 20 houses formerly stood on the castle site, and it is clear from this survey that Huntingdon was a town of considerable size: it had 256 burgesses living in four wards. Though it suffered in the civil wars of Stephen's reign, by the end of the 13th century the town had reached a peak of prosperity. It had the staggering number of sixteen parish churches, and six religious houses (though three were outside the borough boundary).
The growth of civic power is shown by the grant from the Crown to the burgesses of the town of special privileges and liberties in Royal Charter that are still extant. The first grant was by King John in 1205. In 1252 Henry III granted to Huntingdon all the tolls levied on goods brought into St Ives. The expansion of the town came to a halt in the 14th century, when impediments to Ouse navigation and the Black Death hit the town particularly severely. The charter of 1363 states that a quarter of the town was uninhabited. The decay of the borough continued in the 15th century, and at the beginning of Henry VIII's reign half the dwelling houses were empty and the number of parish churches had been reduced to four. This Dissolution of the religious houses led to considerable changes in society, and the rise of the Williams and the Cromwell family. Oliver Cromwell was elected MP for Huntingdon in 1628.
Under a charter of Charles I granted in 1630 the medieval style of the corporation, governed by "Bailiffs and Burgesses", was changed to "The Mayor, Aldermen and Burgesses". Except for a brief period in the 17th century this charter remained in force until 1835. Huntingdon suffered in the Civil War between King and Parliament, and two of the remaining four churches were badly damaged.
The Restoration of Charles II heralded a more prosperous era, for, situated as it is at the junction of several major roads, Huntingdon developed into an important coaching centre in the 16th and 17th centuries. Travellers were catered for in a number of inns, and the houses along the High Street were gradually rebuilt or re-fronted to give the town its characteristic appearance.
The coming of the railway in the 19th century caused an abrupt change in the town's fortunes. The opening of the Great Northern Line in August 1830 meant that rail travel largely superseded travel by road, and this change, coupled with the agricultural depression of the latter part of the 19th century, led to a period of decay - happily reversed in more recent times.
The closed corporation of Huntingdon and the borough of Godmanchester were drastically reformed following the Municipal Corporations Act of 1835. The government of each town then passed to a Mayor, Aldermen and Councillors, and the vote was given to the ratepayers. In 1832 the boroughs were united for Parliamentary purposes. The two boroughs continued as separate entities until 1961, when they were united to form the new borough of Huntingdon and Godmanchester, governed by a Mayor, six Aldermen and eighteen Councillors. The reorganisation of local government which took place in April 1974 saw the County of Huntingdon and Peterborough absorbed into the new enlarged Cambridgeshire. The Town Council continued in being, based in the Town Hall, though several of its functions passed to the new Huntingdonshire District Council, whose headquarters, Pathfinder House, were opened in 1977. In April 1982 Godmanchester secured its own Town Council and Huntingdon was then left with its own local Council with the same boundary as the pre-1961 borough.