It is included in the Federal Aviation Administration (FAA) National Plan of Integrated Airport Systems for 2017–2021, in which it is categorized as a non-hub primary commercial service facility.

In 1925, Lt Harry Warner arrived in Lansing to help Davis and others select the current site for Capital City Airport.

[11] The formal dedication of Capital City Airport was held on the weekend of July 14–15, 1928, and was attended by 70,000 people, including arctic explorer George Hubert Wilkins and aviator Carl Eielson.

Pilots from Selfridge Field and members of the Michigan National Guard 107th Observation Squadron performed in an exhibition air show.

Mayor Laird J. Troyer, Chamber of Commerce President Alton J. Hager, and airport committee chairman Clyde B. Smith, among others, were present to witness the plane's arrival.

Foster completed construction on a 60-by-120-foot, 7,200 square feet (669 m2) aircraft hangar, the first building in what would become known as the Francis Aviation Complex at Capital City Airport.

By 1934, Pennsylvania Airlines and Transport was providing air mail and passenger service to Detroit, Grand Rapids, Muskegon, and across Lake Michigan.

[17] In 1940, the original terminal building, a 100-by-100-foot concrete hangar, and an adjoining office wing at the west end of the airport were built.

[18] The same year, the airport unsuccessfully bid for an $8.4 million Aircraft Engine Research Laboratory of the National Advisory Committee for Aeronautics.

[16] In April 1967, a new $38,000 observation room opened, where viewers can hear radio communications between pilots and the control tower through a loud speaker.

Between 1988 and 1990, runway 14/32 was decommissioned and became taxiway F.[24] In January 1987, United Airlines announced it was ending flights between Chicago O'Hare International Airport (ORD) and Lansing on April 5 after nearly 56 years of service.

[33] In 1992, a major renovation of the terminal building, designed by Greiner, Inc., included the addition of 50,000 square feet (4,645 m2) to the facility, began.

[24] President Bill Clinton landed at the airport aboard Air Force One on July 22, 1999, to hold a forum on Medicare at Lansing Community College.

[45] In July 2004 Independence Air began nonstop flights from Lansing to Washington, D.C.'s Dulles International Airport (IAD).

Independence Air left the Lansing market in January 2005, citing high fuel prices and heavy competition from Northwest.

[52] In January 2008, Kenny Tours announced non-stop flights from Lansing to Shannon, Ireland, dubbed the Shamrock Express, to begin in June 2008.

[54] Apple Vacations announced in July 2009 that, starting in December, they would offer weekly seasonal flights to Cancún, Mexico on USA3000 Airlines.

[60] In October 2010 the airport was awarded a U.S. Department of Transportation Small Community Air Service Development grant, worth $750,000, to help reestablish nonstop flights from Lansing to Washington, D.C.

[37][61][62] In December Sun Country Airlines announced that it would offer non-stop flights from Lansing to Minneapolis (MSP) and Washington–Reagan (DCA) beginning in April 2011.

[65][66] American Airlines resumed the Washington, D.C. flights in July 2016, continuing a slot exemption that Sun Country previously held at Washington–Reagan.

[69][70] President Barack Obama landed at the airport aboard Air Force One on February 7, 2014, to sign the 2014 U.S. Farm Bill at Michigan State University.

[73] A Concierge Travel Center opened at the airport in May 2010, offering the ability to book airline tickets, cruises, tours, car rentals, and hotel rooms.

Lansing is part of Avelo's plan to connect unique city pairs in underserved markets, especially focusing on "small hometown airports."

[83] In October 2018 the airport announced the establishment of a Lansing Brewing Company-themed restaurant and bar, and a new coffee cafe, to open in late 2019.

[87] The Port Lansing Global Logistics center, a $6 million 48,000 square feet (4,459 m2) cargo warehouse and cross-docking facility, opened at the airport in October 2012.

[89] The Concierge Travel Center offers the ability to book airline tickets, cruises, hotels, tours, foreign currency exchange, and limousine rentals.

In addition, the Michigan Flyer provides motorcoach service roundtrip from nearby East Lansing to Detroit Metro Airport 12 times daily.

[108] An April 2011, a New York Times study determined that the average fare from Capital Region International Airport was overpriced by $117.

The regression analysis, based on third quarter 2010 data from the USDOT Bureau of Transportation Statistics, considered factors such as market size and average distance to destination.

Source: Airline Origin & Destination Survey, Office of the Assistant Secretary for Research and Technology, Bureau of Transportation Statistics, USDOT