The origin of the name (along with the surname Cunningham) is uncertain. The ending -hame is Old English hām ("home, village"). The first component may be either Old English cyning, cuning ("king") or Gaelic coineanach ("rabbit"). Irvine, a former capital of Scotland, was the capital of Cunninghame, indicating its status as a royal burgh. The family crest includes the unicorn, which is restricted to the Crown, and Clans Cunningham, Oliphant, and Ramsay.
The historic district of Cunninghame was bordered by the districts of Renfrew and Clydesdale to the north and east respectively, by the district of Kyle to the south over the River Irvine and by the Firth of Clyde to the west.
Cunninghame became one of the three districts or bailieries of Ayrshire, the shire or sheriffdom of Ayr. Cunninghame was in the north, along the River Irvine; Kyle was in the centre, along the River Ayr; and Carrick was in the south, along the River Doon. By the eighteenth century Ayrshire had become one of the counties of Scotland, with the three bailieries being described as "districts" or "divisions" of the county, although they had no formal administrative existence.
In the late nineteenth century the "territorial division" was described as comprising the civil parishes of Ardrossan, Beith, Dalry, Dreghorn, Fenwick, Irvine, North Ayrshire, Kilbirnie, West Kilbride, Kilmarnock, Kilmaurs, Kilwinning, Largs, Loudoun, Stevenston, Stewarton and part of Dunlop.
The name was revived for one of nineteen districts of the Strathclyde region of Scotland, formed by the Local Government (Scotland) Act 1973 in 1975. The district was formed from parts of the counties of Ayr and Bute, namely:
The Cunninghame District Council was granted a coat of arms by Lord Lyon King of Arms in 1979. The main feature of the arms was a black "shakefork" from the arms of Clan Cunningham. To the left was the arms of the former royal burgh of Irvine, based on the crest of the royal arms of Scotland, and said to have been granted to the town by King David I. To the right was an ancient ship which had appeared in the arms of both Bute County Council and Arran District Council. Above the shakefork was a leopard's head holding in its mouth a weaver's shuttle. this represented the weaving industry of the inland parts of the district. Such an emblem appeared in Scottish arms grants to weaving societies and associations, and in the armorial bearings of the Worshipful Company of Weavers of the City of London. The motto was Sense and Worth, and the arms were completed by a gold coronet of a design reserved by Lord Lyon to district councils, topped by thistle-heads.
The district was abolished in 1996 by the Local Government etc. (Scotland) Act 1994, when the system of regions and districts was replaced by unitary council areas. The area of the Cunninghame district (including Arran) became North Ayrshire council area. The name Cunninghame still exists though as two constituencies in the Scottish Parliament, namely Cunninghame North and Cunninghame South.