What became Lincoln Airport began in the early 1920s, when the city selected land northwest of Lincoln for a municipal airfield. Charles Lindbergh received flying instruction in Lincoln in 1922. The airfield became a stop for the predecessor of United Airlines in 1927 and an air-mail stop the following year. United continues to serve Lincoln through United Express.

The Lincoln Airplane and Flying School was established in 1928 and operated at the airfield (which briefly was known as Lindbergh Field), before later moving to Union Airport a few miles east. In 1939, the Lincoln Airplane and Flying School was one of nine civilian contract flight schools contracted by the United States Army Air Corps as Lincoln Army Air Field for basic flight training of air cadets under the 4,500-pilot training expansion program. The school was operated by E.J. Sias. However, due to the short summer flying season, flight training in Lincoln was closed on 15 November 1940 and moved to Drane Field in Lakeland, Florida where it reopened with new owners under the name "Lakeland School of Aeronautics" and continued Army contract pilot training. As part of the contract flying school, the Air Corps established the 47th Training Detachment to command the military flight cadets at the school, which apparently also moved to Lakeland along with the school. The school/base closed in December 1945 and the airport was transferred back to the City of Lincoln.

Along with its civil use, Lincoln Airport became host to a flying unit of the newly formed Nebraska Air National Guard along with a Naval Reserve unit flying patrol aircraft. The 173rd Fighter Squadron became the host unit of what became known as Lincoln Air National Guard Base. Equipped with P-51 Mustang fighters in 1946, it was the second Air National Guard unit established. A few years later, F-80C Shooting Star jet fighters replaced the Mustangs until the advent of the Korean War. The U.S. Navy Reserve also established Naval Air Station Lincoln (NAS Lincoln) on the airport, primarily as home to Patrol Squadron 762 (VP-762) and its P-2 Neptune aircraft.

In 1952, the U.S. Air Force took over the airport as Lincoln Air Force Base, complicating civilian general and commercial aviation in the city. In 1959, the diagonal runway (14/32) was closed. In late 1963, a new 4,000-foot (1,220 m) runway (17/35) parallel to the main runway, with associated facilities for general and commercial aviation, was opened on the east side of the airport to reduce the number of non-military aircraft movements on the main runway. After operating as a Strategic Air Command (SAC) base supporting B-47 Stratojet bombers, KC-97 refueling aircraft (by 1954), and Atlas intercontinental ballistic missiles (by 1962), the Air Force closed the installation in 1966 and returned it to civilian hands.

During the 1960s, the two main airlines at Lincoln were United Airlines and the original Frontier Airlines. Frontier Convair 580s flew nonstop and direct to Denver and Kansas City. United Douglas DC-6Bs flew nonstop to Denver, but nonstops to Chicago didn't start until 1967. Lincoln's first jet service began in 1966, with Frontier Boeing 727-100s operating between Denver and Kansas City via Lincoln. In 1956, runway 14/32 was reopened. United Boeing 727-100s and Boeing 737-200s began flying nonstop to Chicago and Denver about 1968; LNK later saw United 727-200s, 737-300s, 737-500s, and Airbus A320s. Frontier later operated 737-200s.

Other jet service was operated by America West with Boeing 737-200s and 737-300s nonstop to Phoenix and Trans World Airlines (TWA) DC-9s nonstop to St. Louis. In 1983, Midway Airlines was operating Douglas DC-9-10 jets direct to Chicago Midway Airport via a stop in Omaha. By 1985, three airlines were operating jet service into the airport according to the Official Airline Guide (OAG) including Air Wisconsin with British Aircraft Corporation BAC One-Elevens nonstop from Chicago O'Hare Airport and Grand Island, NE, Frontier with Boeing 737-200s and McDonnell Douglas MD-80s nonstop from Denver and Omaha, and United with Boeing 727-100s and Boeing 737-200s nonstop from Chicago O'Hare, Denver, Cedar Rapids, and Peoria. The original Frontier Airlines ceased operations in 1986; successor Continental Airlines flew 737s and DC-9s to Denver. United mainline jet service was eventually replaced by flights operated by its United Express partners, who now fly 50-seat regional jets from LNK.

In 2005, Northwest Airlines flew to Memphis but dropped the route within nine months. In early 2006, Allegiant Air began air service to Las Vegas but after two years, announced that it was transferring service to Grand Island, NE. In May 2014 Delta Air Lines announced a non-stop flight to Atlanta would start September 8, resuming a service it briefly ran in 2009. In 2011 Delta resumed the Memphis service, but only over the summer. $750,000 in federal spending was used to guarantee revenue for Delta.

Today, part of Lincoln Airport hosts the Air National Guard's 155th Air Refueling Wing (155 ARW), an Air Mobility Command (AMC)-gained Air National Guard unit flying the KC-135R Stratotanker.