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The 747-400F (Freighter) is an all freight version of the 747-400. While using the updated systems and wing design of the passenger versions, it features the original short upper deck found on the classic 747s to reduce weight. The 747-400F has a maximum takeoff weight of 875,000 pounds (397,000 kg) and a maximum payload of 274,100 pounds (124,000 kg). The -400F can be easily distinguished from the passenger -400 by its shorter upper-deck hump and lack of windows along the main deck.

The model's first flight was on May 4, 1993, and entered service with Cargolux on November 17, 1993. Major customers included Atlas Air, Cargolux, China Airlines, Korean Air, Nippon Cargo Airlines and Singapore Airlines.

The 747-400F has a main deck nose door and a mechanized cargo handling system. The nose door swings up so that pallets or containers up to 40 ft (12 m) can be loaded straight in on motor-driven rollers. An optional main deck side cargo door (like the 747-400M Combi) allows loading of dimensionally taller cargo modules. A lower deck (belly) side door allows loading of unit load devices (ULD) up to 163 cm in height.