The 747-400 was announced by Boeing Commercial Airplanes in October 1985. Compared to the 747-300 the 747-400 has 6 feet (1.8 m) wing tip extensions and 6 feet (1.8 m) winglets, and a glass cockpit which dispensed with the need for a flight engineer. The 747-400 also improved on the -300 with tail fuel tanks, revised engines, an all-new interior, revised fuselage/wing fairings and newer in-flight entertainment. Like the 747-300, the passenger version of the 747-400 included the stretched upper deck (SUD) as a standard feature. The SUD was almost twice as long as the standard upper deck. It had previously been offered as a retrofit and first appeared on two Japanese 747-100 SR models. While the wingspan was increased, the overall weight of the wings was decreased due to the use of composites and aluminum alloys.

It was rolled out in January 1988 and first flew on 29 April 1988. Certification was received on 10 January 1989 with Pratt & Whitney PW4000 engines, 18 May 1989 with CF6-80C2s and 8 June 1989 with Rolls-Royce RB211-524Gs. The first 747-400 was delivered to Northwest Airlines on 26 January 1989, with service entry on 9 February.

The extended range freighter (ERF) entered service in October 2002. The next month, the extended range (ER) passenger version entered service with Qantas, the only airline ever to order the passenger version of the 747-400ER. Qantas uses the aircraft on its Melbourne-Los Angeles and Sydney-San Francisco flights, which are too long to operate using a standard 747-400.

The Boeing Signature Interior was later made available on the 747-400, either as interior refitting on existing 747-400s or as a "fresh-from-installation" option on newer 747-400s and 747-400ERs. One example, China Airlines's four newest Boeing 747-400s (tail number B-1821x), also the last four passenger 747-400s built, were newly built with Boeing Signature Interior. One of these (B-18210) has a hybrid livery, with China Airlines' tail and Boeing's fuselage liveries.

The 747-400 is an improved version of the 747-300 with increased wingspan, winglets, revised engines and a glass cockpit that removed the need for a flight engineer. The 747-400 passenger version features a stretched upper deck (SUD) like the 747-300 as a standard feature. In 1989, a Qantas 747-400 flew non-stop from London to Sydney, a distance of 9,720 nmi (11,190 mi, 18,000 km) in 20 hours and 9 minutes, although this was a delivery flight with no commercial passengers or freight aboard and using extra dense jet aviation fuel produced specially by Shell.

Production of the 747-400 passenger version officially ceased on 15 March 2007.The last four -400s on order were canceled by Philippine Airlines (which switched to the 777-300ER). The last to order the -400 was China Airlines in November 2002, with the last passenger 747-400 constructed in 2005 and delivered in April of that year. It was the 1358th 747 (MSN33737/B-18215).