The F-35 beat rivals Boeing F/A-18 Super Hornet and the European-made Eurofighter to replace the air force's aging F-4 fighters.
The purchase, estimated at around $7 billion for 42 planes, will be a welcome boost to the fortunes of Lockheed Martin and a welcome addition to Japan's armory during uncertain regional political times.
Tokyo's decision comes as the region considers the repercussions of the death this week of North Korean leader Kim Jong Il. His authority passes to his youngest son, Kim Jong Un, who remains little known by Western governments.
Although he has a high military rank, the younger Kim's attitudes and relations with the military are unclear. There is much speculation about how much authority he will have over the military in a country suspected of having nuclear capabilities.
Some nuclear analysts suspect Pyongyang may have enough plutonium to arm about a dozen weapons.
"The security environment surrounding future fighter jets is transforming," Japanese Defense Minister Yasuo Ichikawa said. "The F-35 has capabilities that can firmly respond to the changes."
The decision was formally made at the Security Council of Japan, led by Prime Minister Yoshihiko Noda, as well as at a meeting of Noda's Cabinet, a report by Kyodo news agency said.
''Over the future, we want our aircraft to be equipped with qualities that can deal properly with the various changes facing our security environment,'' Ichikawa said.
The F-35A conventional takeoff and landing variant was offered by the U.S. government with participation from Lockheed Martin. The initial contract will be for four jets delivered sometime in Japan's fiscal year, which starts in April, a statement from Lockheed Martin said.
"We are honored by the confidence the Japanese government has placed in the F-35 and our industry team to deliver this fifth-generation fighter to the Japan (air force)," Bob Stevens, Lockheed Martin chairman and chief executive officer, said. "This announcement begins a new chapter in our long-standing partnership with Japanese industry and builds on the strong security cooperation between the United States and Japan."
The F-35 program has nine partner nations -- the United States, United Kingdom, Italy, Netherlands, Turkey, Canada, Australia, Denmark and Norway.
Japan isn't a partner nation but Lockheed is offering final assembly work in-country as well as some component and sub-component assembly. Japanese firms Mitsubishi Heavy Industries and IHI Corp. will participate in the production of the F-35. IHI is a maker of ships, aero-engines and turbochargers.
The United States intends to buy more than 2,440 of the F-35 planes at an estimated cost of $323 billion, making it the most expensive defense program in U.S. history.
Lockheed said the United Kingdom and Netherlands have ordered test aircraft and Italy and Australia have committed long-lead funding for their initial operational aircraft.
In October 2010, Israel selected the F-35A as the Israel air force's next generation fighter and is scheduled to receive the F-35 through the U.S. government's Foreign Military Sales process.