The first flight landed at what was then known as Ronaldsway Farm in 1928 with commercial aviation growing from the following year. Prior to World War II, Ronaldsway Airport was policed by the Isle of Man Constabulary (IOMC) as part of the general patrol plan for the area. During the War the Airport was taken over for military use, only returning to civilian ownership in 1948 when the Airport was sold by the Admiralty to the Isle of Man Government for £200,000.

In 1949, Acting Sergeant A P Cowin of the IOMC was posted from St Johns to head the IOMC unit at Ronaldsway Airport. This team would later be headed by Sergeant Stanley White who left the IOMC to remain at the Airport after the Isle of Man Airport Police were formed in 1964.

The IOMC Officers stationed at the Airport after World War II lived with their families at the Airport in "Nissen Huts" formerly used by the Royal Navy. Shortly after the War, there were seven Officers and their families residing at the Airport:

The Policemen of the era lead us to believe that, if an IOMC Officer fell out of favour with the hierarchy, a posting to the Airport may have been used as a way of informally penalising said Officer. However, most who served at the Airport seem to have volunteered so the accuracy of the former statement is unconfirmed.

Incidents handled by the IOMC Police Officers at the Airport in the 1950s included in January 1952, when the offices of the Manx Air Charter caught fire the alarm was raised by Constable Brew who was on Airport patrol and called out the Castletown fire brigade who promptly arrived on site and extinguished the blaze. In November 1954, a RAF helicopter was sent to answer a medical SOS call on the Calf of the Man. Due to the bad weather a radio relay was set up manned by a Constable of the IOMC stationed at the Airport.

The Civil Aviation Act 1949 provided the power to appoint Special Constables on any premises vested or under the control of the Minister of Civil Aviation. This Act was extended to the Isle of Man with the Civil Aviation Act (Isle of Man) Order 1952 but notably, Section 37, which specified the power to appoint such persons was not extended to the Isle of Man. It was not until 1964 that the Airport duties were relinquished by the IOMC with Police Officers separately sworn in for the purposes of enforcing the airport byelaws, etc., this responsibility coming under separate legislation at that time. On 1st April 1964, the Isle of Man Airport Police were formed and took up their duties. Their uniform was in RAF Blue and they wore a winged cap badge, both of which distinguished them from the Officers of the Isle of Man Constabulary.

The Airport Police changed to Aviation Security prior to 1999, possibly as early as the time of the disbanding of the Isle of Man Harbour Police in 1995. The reorganisation of the Service changed the roster pattern as well as the pay and conditions, as all staff from then on were on lower pay. Officers were now titled Aviation Security Officers (ASO). Officers of the Airport Police held Constables warrants, with those prior to the change to Aviation Security being all-island whereas those of subsequent Officers were only for the Airport and surroundings.

The role became pure aviation security at this time but there was a movement to broaden to a Police Service with input from IOMC, Customs, Immigration and the Department of Environment, Food and Agriculture (DEFA), the timing of which was possibly in 2007 with the activities noted below. This included a change of uniform to Police black with the primary difference in uniform from the IOMC, other than the patterns of the metal insignia worn, then being the wording 'AIRPORT' in reflective blue on the back of the outer wear instead of 'POLICE'. The Airport Officers took part in Police training including the use of handcuffs, restraints, taking statements, handling of evidence, Proceeds of Crime Act, 2002 (POCA), etc.

In early 2007, in readiness for the new Air Navigation Order which was to come into effect on the 1st May, Officers undertook a period of training delivered by the Astra Consulting Group, which also ran courses for the Isle of Man Constabulary. The instruction provided covered general policing but specialised in aviation related areas. They also took training from the Coroner's Office and were authorised to act on behalf of the Office at the Airport. They were then sworn in by Sally McMullen, Deputy Chief Registrar, as Commissioner of Oaths.

Their main duties were:

The Service now comprised thirteen Constables, led by a team of Managers who were also sworn in. Cover was provided 24/7, 365 days a year, with a minimum of three Officers on duty during opening hours. There was an Airport aviation security office located on the Airport estate from where the Service operated.

The Aviation Security Officers at the Isle of Man Airport were disbanded at the end of September in 2019, with Officers either taking redundancy or alternative employment within Government or with the contract security company responsible for airfield security after that date. Going forward from this time, the range of duties carried out by the private contract company is limited in part due to their officers not being warranted.