The airport is built on a landfill at the mouth of the Eyjafjarðará River, and was taken into use with installed runway lighting on 5 December 1954. In the beginning, the surface was gravel but in 1967, the runway was paved with asphalt. Earlier, an airport at Melgerðismelar in Eyjafjörður fjord was used, and seaplanes also landed on Akureyrarpollur. Scheduled flights began between Akureyri and Reykjavik in 1937. In 2009, the runway was extended and paved and now measures 2.400 metres.
A new air terminal was taken into use in 1961. The terminal has been expanded twice and significant improvements were made to the older part of the terminal in 2000. The size of the passenger area is 550 square metres, which can be divided into three halls when required by international flights. A cafeteria with a spacious dining area is in the waiting hall. The waiting hall also includes an ATM and a duty free store for international passengers.