Although technically the Air Force One designation applies to the aircraft only while the president is on board, the term is commonly used to refer to the VC-25 in general.

The two aircraft often operate in conjunction with Marine One helicopters, which ferry the president to airports whenever a vehicle motorcade would be inappropriate.

By 1985, the pair of Boeing 707-based VC-137s used as the presidential aircraft had been in service for 23 and 13 years respectively, and the USAF began searching for an eventual replacement.

The Request for Proposal issued stated that the aircraft to be selected should have at least three engines and an unrefueled range of at least 6,000 miles (9,700 km).

[3] Problems with interior wiring for communication systems delayed delivery of the two aircraft until 1990,[2] during the administration of George H. W. Bush.

While the VC-25 has two main decks and a cargo area, like a regular Boeing 747, its 4,000 square feet (370 m2) of floor space has been reconfigured for presidential duties.

[7] However, the aircraft also has built-in airstairs that lead to the lower deck, typically used when security concerns make the use of a mobile stairway impractical.

This capability was added after the September 11 attacks, during which the aircraft had to land at Barksdale Air Force Base for President George W. Bush to address the nation.

[6] There are separate quarters for guests, senior staff, Secret Service and Air Force security personnel assigned to the plane, and the news media located in the aft area of the main deck.

[6] While the aircraft's luggage capacity is adequate to carry the belongings of the passengers, the logistics train of the president means that the aircraft must fly preceded by an aerial convoy of several cargo transports, which carry the helicopters, motorcade vehicles, and other equipment required by the presidential entourage.

[13] After a presidential inauguration resulting in a change in office, the outgoing president is provided transport on a VC-25 aircraft to their home destination.

[14][15] The VC-25As have also been used to transport deceased former presidents, as the guest area aft of "the White House" has chairs and tables that can be removed and the casket laid in their place.

[6] A specially designed hydraulic lifter (similar to the type used by airline catering) with the presidential seal affixed to the sides lifts the casket up to the portside aft door to enter the VC-25A.

Boeing was awarded a contract in January 2016 to identify cost reduction opportunities in areas including maintenance, aerial refueling and communications.

[30] On 1 August 2017, Defense One reported that in an effort to pay less for the replacement program, the USAF entered into a contract to purchase two 747-8 Intercontinental (747-8I) jets from Boeing, which had originally been ordered in 2011 by Transaero, a Russian airline.

Before they could be delivered, Transaero filed for bankruptcy and was closed down; the two aircraft were stored at Southern California Logistics Airport in the Mojave Desert to prevent corrosion.

[32] In April 2022, Boeing's CEO Dave Calhoun revealed that he expects the company to have a loss of $660 million on the VC-25B program, after the contract was renegotiated by President Trump.

While the jacking did not result in damage to the planes, "the Pentagon's contractor-management agency formally requested Boeing improve its operations.