That relationship was shaken last week when Japan Airlines announced a blockbuster deal to buy A350 jets from Airbus.
But the Boeing-Japan fortress isn't about to crumble quickly, close observers say.
Near term, party politics in Japan give Boeing an edge over Airbus for a pending big jet order by the second big Japanese airline, All Nippon Airways.
And Japanese manufacturing partners will likely supply all the fuselage panels on Boeing's soon-to-be-launched 777X program, just as they do for today's 777.
Long term, though, Airbus should gain further market share in Japan, and the dual sourcing by the airlines could spread to the Japanese manufacturers.
"There is no agreement between Japan and Boeing that we will cooperate forever," said Norio Yamanouchi, who played a lead role in developing the close relationship between Boeing and Japan. "It might not be a bad idea for Japan to work with Airbus on future airplane programs."
A former top Boeing executive, who still works in aviation and asked for anonymity, said "it's inevitable Airbus will continue to chip away at Boeing's dominance in Japan."
Nevertheless, said analyst Adam Pilarski of consulting firm Avitas, Japan's big aircraft-parts manufacturers -- especially Mitsubishi, Kawasaki and Fuji, the three "heavies" -- remain "super critical to Boeing."
Yamanouchi, who is 73, has a unique perspective. Working for the Japan Aircraft Development Corp. in Seattle, he helped Boeing win JAL and ANA as launch customers for the 767 and 777 jets in return for Japan's industrial participation in those programs.
In 2005, Airbus made him a senior adviser in its campaign to break Boeing's stronghold. He left Airbus in 2009 and now consults for other aviation businesses from Tokyo.
Yamanouchi said he expects ANA will order Boeing's 777X rather than follow JAL.
ANA could be tempted by Airbus, he said, because it faces the prospect of rival JAL flying new fuel-efficient A350s several years before ANA can get 777Xs.
But he believes ANA would face huge operational costs in adding Airbus planes, which have very different cockpits and require separate pilot and maintenance training.
In addition, he said, there is the reality of Japanese politics. While JAL was in bankruptcy two years ago, the ruling Japanese Democratic Party gave the airline substantial financial support.
The Liberal Democratic Party that returned to power in Japan last year has shown "a tight political connection" with ANA, Yamanouchi said.
He said the government wants airlines to buy the Boeing 777X because Japanese industry will help build it.
"It is very difficult for a big business in Japan to do something that goes against the Japanese government's desire," Yamanouchi said. "If ANA buys the A350, the Japanese government will lose face."
The former Boeing executive agreed, citing the "very subtle pressure at the very top levels between companies and between government and companies" in Japan.
"We certainly relied on that to influence JAL and ANA to be launch customers when we launched the 787," he added.
Out of favor with the current government, JAL resisted the pressure to buy Boeing.
Last week, in what could be seen as sign of disfavor, the Japanese government awarded ANA 11 valuable slots at Tokyo's expanded Haneda airport, granting JAL just 5.
Yamanouchi thinks that for now Boeing still needs Japan's manufacturing skills.
"A major reason Boeing has been working with Japanese industry is because of its capability," he said. "Its market dominance with JAL and ANA is a byproduct, not the primary reason."
And investment by Japanese manufacturing partners reduces Boeing's development costs.
If Japan hadn't been willing to build 35 percent of the 787 airframe, Boeing might have had difficulty in getting the program off the ground, he said.
Yamanouchi expects Boeing to maintain Japan's 777 work share for the new 777X, in part to shore up the program's credibility with global airlines.
But for future airplane programs, starting with the 737 replacement sometime after 2020, prospects are unclear. He suggested that Boeing might seek to cultivate other partners, including China.
Until then, Boeing still needs Japan. John Byrne, Boeing vice president for procurement, said this year that the jet-maker buys commercial and defense parts from Japan worth $2.5 billion annually.
Conner, speaking last year to a gathering of Japanese Americans, echoed the 787 tagline from a series of Boeing ads and an ANA promotional video: "This aircraft is 'Made with Japan.'"
Pilarski attributes JAL's decision to order from Airbus largely to the airline's frustration with years of 787 delays, the months-long grounding and in-service glitches that have shown up since.
Just last week, separate systems faults forced two more JAL 787 flights to turn back in the air, for a total of seven since the planes resumed service in June.
"The Japanese take face and trust very seriously. If the Japanese promise something, that is gold," Pilarski said. "But that works both ways. They expect you to deliver."
He said Boeing must now restore its reputation for reliability, starting with the 777X.
The Airbus A350, by having its first flight in Paris in June, "passed the first test -- not being really late," he said.
But this short-term advantage may disappear. He said airlines he has spoken to are excited about 777X and believe it will prove the superior airplane.
The former Boeing executive heard similar comments from senior airline management, including at Emirates, which is expected to be the 777X launch customer next month.
Ultimately, the executive said, the JAL loss "might be good for Boeing," ensuring a new focus on getting 777X launched.