The constituency of Huntingdon has existed in three separate forms: as a Parliamentary Borough from 1295 to 1885; as a Division of a Parliamentary County from 1885 to 1918; and as a County Constituency from 1983 until the present day.
Representatives for the seat, the standard two burgesses per parliamentary borough, were summoned to form the first fully assembled parliament, the Model Parliament in 1295 and at all parliaments assembled from then until 1868, in which year the constituency was reduced to a single-member Borough in accordance with the Reform Act 1867. In the mid-17th century, this was Oliver Cromwell's constituency.
Under the Redistribution of Seats Act 1885, the Parliamentary Borough was abolished altogether and the two-member Parliamentary County of Huntingdonshire was replaced by the two-single member seats formally known as the Northern or Ramsey Division and the Southern or Huntingdon Division. It was abolished under the Representation of the People Act 1918 when it was re-combined with Ramsey and Huntingdonshire was re-established as a single member constituency.
The former Conservative Prime Minister (1990–1997) John Major represented the seat from its re-creation in 1983 until his retirement in 2001. His majority in 1992 (36,230) was the largest majority for any member of parliament post-1832 until 2017, in which George Howarth won a 42,214 vote majority in Knowsley.
1832-1885: The townships of Huntingdon and Godmanchester.
1885–1918: The Sessional Divisions of Leightonstone and Toseland, incorporating the towns of Huntingdon, Godmanchester, and St Neots.
1983–1997: The District of Huntingdon wards of Brampton, Bury, Earith, Ellington, Elton, Farcet, Fenstanton, Godmanchester, Hemingford Abbots and Hilton, Hemingford Grey, Houghton and Wyton, Huntingdon North, Huntingdon West, Kimbolton, Needingworth, Ramsey, Sawtry, Somersham, Stilton, St Ives North, St Ives South, The Stukeleys, Upwood and The Raveleys, Warboys, and Yaxley, and the City of Peterborough wards of Barnack, Glinton, Northborough, Werrington, and Wittering.
1997–2010: The District of Huntingdonshire wards of Brampton, Buckden, Eaton Ford, Eaton Socon, Ellington, Eynesbury, Fenstanton, Godmanchester, Gransden, Hemingford Abbots and Hilton, Hemingford Grey, Houghton and Wyton, Huntingdon North, Huntingdon West, Kimbolton, Needingworth, Paxton, Priory Park, St Ives North, St Ives South, Staughton, The Offords, and The Stukeleys.
Gained the parts of the District of Huntingdon, including St Neots, which had previously been part of the abolished South West Cambridgeshire constituency. The City of Peterborough ward of Werrington was transferred to the Peterborough constituency. Remaining Peterborough wards and northern parts of the District of Huntingdon, including Ramsey, were included in the new County Constituency of North West Cambridgeshire.
2010–present: The District of Huntingdonshire wards of Alconbury and The Stukeleys, Brampton, Buckden, Fenstanton, Godmanchester, Gransden and The Offords, Huntingdon East, Huntingdon North, Huntingdon West, Kimbolton and Staughton, Little Paxton, St Ives East, St Ives South, St Ives West, St Neots Eaton Ford, St Neots Eaton Socon, St Neots Eynesbury, St Neots Priory Park, and The Hemingfords.
Local authority wards revised. Further minor loss to North West Cambridgeshire.
^As with all constituencies, the constituency elects one Member of Parliament (MP) by the first past the post system of election at least every five years, though this was not the case in its first creation