The town was once a haunt of Robert Burns, after whom two streets in the town are named: Burns Street and Burns Crescent. Despite being classed as a new town, Irvine has had a long history stretching back many centuries and was classed as a Royal Burgh. There are also conflicting rumours that Mary, Queen of Scots was briefly involved in the town's history. Some say she stayed briefly at Seagate Castle. To this day there is still an annual festival, called Marymass, held in the town. It is the birthplace of the present Deputy First Minister of Scotland, Nicola Sturgeon and the former First Minister of Scotland, Jack McConnell. Its twin town is Saint-Amand-les-Eaux in northern France just outside Lille.

Irvine was granted its first Burgh Charter in around 1249. This entitled the town to organise its own affairs under a Town Council. In circa 1372 a dispute arose between Irvine and Ayr as to which of the two burghs had rights to control trade in the Barony of Cunninghame and Barony of Largs. The Burgesses of Irvine were able to produce Royal Charters showing that the town had the right to control trade in the Baronies of Cunninghame and Largs. The dispute was resolved by Robert II's Royal Charter of 8 April 1372 conferring Royal Burgh status.

Originally Fullarton remained outwith the Royal Burgh of Irvine as a distinct village and latterly burgh in its own right in the Parish of Dundonald until the Irvine Burgh Act 1881 extended the town's boundaries.

Irvine continued to administer itself with the usual Royal Burgh administrative arrangements of Provost, Bailies and Burgesses. Responsibility for public health, schools and strategic services such as roads passed to Ayr County Council in 1930 when the town was re-classified as a Small Burgh. On 16 May 1975 the Royal Burgh of Irvine Town Council was abolished and its functions were transferred to the now defunct Cunninghame District Council. One of the last acts of the old town council was to present the bulk of the Royal Burgh records and the Provost's regalia to the Irvine Burns Club Museum on Eglinton Street.

There is a Community council in Irvine. However, unlike counterparts elsewhere in Scotland, it opts not to use 'Royal Burgh of' in its title.

The motto used on the coat of arms of the Royal Burgh is 'Tandem Bona Causa Triumphat.' This means the Good Cause Triumphs in the end

The harbour for Irvine has a long history and once was one of the most prominent ports in Scotland after Glasgow. Across from the main harbour itself there was a terminal for the ICI-Nobel Explosives plant on the River Garnock. Much of the harbour went into decline in the 19th century when Glasgow, Greenock and Port Glasgow achieved higher prominence as sea ports. Despite this, there was still commercial sea traffic, though the harbour went into further decline in the 20th century. The main shipping in the 20th century was light coastal traffic and vessels destined for the Nobel Explosives facility. This facility had its own quay, which, although now disused, is still visible from Irvine Harbour. A shipyard on the River Irvine, the Ayrshire Dockyard Company, remained active until after World War II, though its last ship was built just prior to the war.

Afterwards it was involved in refitting ships and also in the manufacture of fittings for other vessels including the Cunard liner Queen Elizabeth 2. Irvine Harbour is now officially closed as a commercial port and houses a small number of privately owned pleasure craft. It is also home to part of the Scottish Maritime Museum with numerous vessels on display, including the 'Spartan', one of the last surviving Clyde puffers.