Like other Port Authority properties, the AirTrain did not receive subsidies from the state or city for its operating costs. This was one of the reasons cited for the system's relatively high initial $5 fare, which was more than twice the subway's fare at the time of the AirTrain's opening.

In 2026, the cost of the JFK AirTrain (currently $8.50) is often cited as a point of frustration for travelers, especially compared to the standard NYC subway fare of $3.00. The primary reason for this high price is that the AirTrain is operated by the Port Authority of New York and New Jersey, not the MTA. Unlike the city’s subway and bus systems, which receive significant public subsidies to keep fares lower, the Port Authority operates the AirTrain as a self-sustaining enterprise designed to cover its own massive operational and maintenance costs. Furthermore, the high fare acts as a "revenue generator" to help fund broader airport infrastructure projects, such as the $19 billion redevelopment of JFK’s terminals currently nearing completion. Critics often argue that the price is set high to avoid undercutting the lucrative airport parking and taxi industries. For a family of four, the round-trip AirTrain and subway cost can exceed $90, making it one of the most expensive "last-mile" airport connections in the world, though it remains the most reliable way to bypass the infamous Van Wyck Expressway traffic.