Construction started in 1965 on a new airport to handle travel to nearby naval bases. The new airport was dedicated on September 1, 1968, replacing Imeson Field which carried the same IATA code of JAX. Terrain precluded lengthening the runways at Imeson, a necessity with the inception of commercial jet airliners. A new idea at JIA was separating departing and arriving passengers on different sides of the terminal. This is no longer the case, and the airport now uses the more typical layout with departing passengers on an upper level with an elevated roadway, and arriving passengers on the lower level.

The new airport was slow to expand, only serving two million passengers a year by 1982, but it served over five million annually by 1999 and an expansion plan was approved in 2000. The first phase, which included rebuilding the landside terminal, the central square and main concessions area, as well as consolidating the security checkpoints at one location and adding more parking capacity, was completed in 2004–2005. In 2007, 6,319,016 passengers were processed.

The second phase of the expansion program was carried out over three years, commencing in mid-2006 and projected to cost about $170 million. Concourses A and C were completely rebuilt; the former concourses were demolished. Work on Concourse B was given a low priority because the capacities of the rebuilt Concourses A and C were more than adequate for existing demand. The expansion was designed by Reynolds, Smith & Hills (RS&H).

The economic downturn of 2009 caused a decrease in passengers and flights. This led the JAA to commence the demolition of Concourse B in June 2009 because it was safer and easier for the contractor. After the debris was removed, asphalt was laid to provide space for ground equipment parking. The concourse will be rebuilt when passenger traffic increases, which the JAA had originally projected would occur in 2013 but did not materialize. A section of the old concourse eventually became part of an airline club lounge which opened in 2019.