The first aerodrome in Whangārei was located on Pohe Island in the upper reaches of Whangārei Harbour. Sir Charles Kingsford Smith's aircraft, the Southern Cross, landed on Pohe Island in 1928. This airstrip was not of high quality due to it being built on boggy reclaimed land, so a more suitable site was required. Another site was considered, at Kensington Park, but in May 1939 the current site was opened at Onerahi.

With the outbreak of World War II, immediately after the establishment of the airfield, the airport was taken over by the RNZAF to serve as a training base which became RNZAF Station Onerahi. Flight Lieutenant "Lou" Gates became one of the station commanders. Pilots practised bombing raids on the nearby Matakohe Island and Rat Island. The airport was established with three grass runways. No. 20 Squadron RNZAF was formed there in August 1942 with Hawker Hind biplanes, personnel and aircraft provided from No. 6 (AC) Squadron RNZAF at Milson, Palmerston North. The squadron was disbanded in July 1943 but reformed elsewhere later in the war. The station was reduced to two runways (06/24 and 32/14) shortly after the war and converted for public use. Some of the old airforce barracks are still present today, having been converted into residential properties.

National Airways Corporation (NAC) began twice-daily commercial flights between Whangārei and Auckland in 1948 using Lockheed Electra 10-seat aircraft. NAC replaced the Electra in March 1950 with small de Havilland Dominie 6-seat aircraft as the airport was too small to handle the new Lockheed Lodestar. The de Havilland's small size meant it serviced Whangārei with six return flights daily from Auckland. 10,148 people flew to and from Whangārei in 1950. The 06/24 runway was upgraded and sealed in December 1963 to its current length of 1097m, which allowed NAC to commence commercial flights with the much larger DC3s. A new airport terminal was built on the northern side of the main runway to cater for future growth. A new control tower was also built. The larger capacity of the DC3 meant Whangārei was serviced only twice-daily to Auckland, with some flights continuing north onwards to Kaikohe or other Northland airports.

In August 1970, NAC replaced its DC-3 service to Whangārei with larger Fokker Friendships. Northern Districts Aero Club introduced a twice-daily return air taxi service to compete and provide additional frequency to Auckland on each Monday, Wednesday and Friday. The service, which operated under the name of Executive Air Taxis, started on 21 August 1970 using a newly imported Piper Cherokee Six. This service proved to be popular and was expanded by the end of 1974 to offer a twice-daily Monday to Friday morning and afternoon return services to Auckland. Northern Districts Aero Club was able to fund new clubrooms and a hangar in 1977.

In 1988, NAC's successor Air New Zealand announced the withdrawal of its twice-daily Friendship service in favour of its newly purchased subsidiary Eagle Airways offering up to five Embraer Bandeirante flights a day through Air New Zealand Link. This led to the decline and eventual end of the Northern Districts Aero Club scheduled flights to Auckland. The control tower was closed in 1988 due to nationwide budget cuts, deregulation and as the airport was deemed too small require this service.

In 1991, a new airline, Ansett New Zealand, began flying to Whangārei in competition with Air New Zealand Link. Both airlines flew Bandeirantes, with Ansett also flying Dash 8s. The terminal was upgraded due to this growth.

In September 1998, Ansett New Zealand withdrew its service. To help meet the demand for additional seats, Eagle Airways increased its services by 14 per week to bring the number of Bandeirante flights to Whangārei to 69. This compared with Air New Zealand's previous service of 14 Friendship flights a week. The link flights acted as a more of a shuttle service between Whangarei and Auckland- high frequency on smaller sized aircraft. This proved popular as flights were operated consistently throughout the day and accommodated more passengers' needs.

In 2001, Eagle Airways purchased 16 new Beechcraft 1900D aircraft and begun using this aircraft on all routes, retiring the Bandeirante aircraft. It was able to introduce new services with the improved aircraft and in 2002 begun direct flights linking Whangārei to Wellington. This service operated twice every week day (until 2009 when it was reduced to one) and was Eagle Airways' longest regular flight service at 626 km (90 minutes).

In 2007, Sunair begun daily air services between Whangārei, Tauranga, Rotorua and Napier. This service was discontinued in 2009. Sunair returned to Whangārei in 2015 with a Whangārei to Whitianga via Claris service. This service ceased at the end of 2015 after low patronage. Sunair currently operates scheduled services from Whangarei to Great Barrier and Tauranga

In 2008, Salt Air begun an "xpress" service between Kerikeri, Whangārei and Auckland. These flights landed at North Shore and transferred passengers to Auckland CBD within 60 minutes of leaving Whangārei.