[10] The completed airfield was officially designated as open to use by the public on December 10, 1944, by the Civil Aeronautics Authority (CAA).

A temporary structure housed airport staff at the time of designation, set to be replaced with a $60,000 terminal building following the conclusion of the war.

[11][12] The first scheduled flight arrived in Columbus at 3:08 pm as a stop on a route from New York to Houston in a Ryan Brougham.

[13] Following approval by the Civil Aeronautics Board in April 1947, Delta Air Lines initiated services using the Douglas DC-3 to the airport on July 1, 1947, as a stop along a route from Atlanta to Fort Worth.

The first of these was Atlantic Southeast Airlines (ASA), which got its start operating five flights from Columbus to Atlanta on June 27, 1979, using a fleet of three de Havilland Canada DHC-6 Twin Otters.

The event had raised over a million dollars for local youth charities over its 21-year run, but was finally ended due to high operational costs and a decline in sponsors.

The 2021 project increased the capacity of the terminal building for airline operations and added seating throughout the airport including an indoor aircraft viewing area.

[34] This was temporarily effective as American Eagle began daily services to Charlotte and Dallas–Fort Worth after eight years of not serving the airport;[35] however, the services only lasted from August 2021 to April 2023 with American citing a shortage in pilots and the end of payroll support grants distributed during the COVID-19 pandemic as the reason behind their withdrawal.

The construction will prohibit the use of the airport for military and commercial operations for 103 days, including Delta Connection flights.

The landside portion of the airport has amenities, airline and car rental check-in counters, a baggage claim conveyor, and an aircraft viewing area.

[34][46] The airport has a rotating beacon, illuminated wind cone, automated surface observing system (ASOS), and a control tower.

[44] Columbus Airport has historically provided passenger, cargo, and charter flights to several destinations in the Eastern United States.

Route 10 of the METRA Transit System serves a bus stop along Airport Thruway at a nearby Walmart on an hourly basis.

[52] In the year ending November 30, 2022, the airport had 37,662 aircraft operations, with an average of 103 per day: 86% general aviation, 7% air taxi, 3% airline, and 4% military.