The new airport was dedicated on September 1, 1968, replacing Imeson Field which carried the same IATA code of JAX.

[4] Terrain precluded lengthening the runways at Imeson, a necessity with the inception of commercial jet airliners.

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 more parking capacity was completed in 2004–2005.

The concourse will be rebuilt when passenger traffic increases, which the JAA had originally projected would occur in 2013 but did not materialize.

In 2019, RS&H and Jacobs Engineering were chosen to perform the design, while Balfour Beatty was selected as the construction manager for the concourse B project.

Past baggage claim and ticketing is the mezzanine, where shops, restaurants and the security checkpoint are located.

In the year ending February 28, 2023, the airport had 99,616 aircraft operations, an average of 273 per day: 63% scheduled commercial, 19% general aviation, 14% air taxi and 4% military.

Military Construction (MILCON) funds provided for the establishment of Jacksonville Air National Guard Base in the southwest quadrant of the airport and placement of USAF-style emergency arresting gear on the JAX runways.

[16] The 2023 fiscal year (10/1/2022-9/30/2023) set a record for passenger numbers at Jacksonville International Airport.

[50] On December 6, 1984, Provincetown-Boston Airlines Flight 1039 crashed on takeoff, killing 11 passengers and 2 crew on board.

The 1986 National Transportation Safety Board report cited elevator trim control system failure, causing separation of the horizontal stabilizer.