The $55 billion bomber program aims to develop a long-range strike aircraft to replace the B-2 Stealth bomber.
Air Force spokesman Ed Gulick said the Pentagon wants the initial aircraft in the mid-2020s. The Pentagon will order 100, he said, implying a price tag of $550 million per bomber.
The first version of the bomber will be piloted, Gulick said, "but it will be provisioned to enable future unmanned capability."
The Pentagon's precise requirements are classified, he said.
The agreement between the two defense giants names Boeing as the prime contractor and Lockheed Martin as the primary teammate.
The two companies first announced a partnership to go after the Air Force's future long-range strike requirement in January 2008, with a declared target to provide the bomber capability by 2018.
However, in 2010 the two suspended their partnership after the Pentagon put the bomber program on indefinite hold.
Now, despite the current budget squeeze, the Defense Department wants to get things moving again.
"The partnership has been reignited and restructured to fit the current requirements of the Air Force program," said Boeing spokesman Todd Blecher. "We didn't just hit the pause button and then play. The program requirements have evolved and the way this team will work has evolved."
In the past, big Pentagon procurement programs have led to ballooning costs and huge delays in getting weapons systems operational.
The B-2 Stealth bomber, the most advanced long-range bomber now available, started as a classified program in the late 1970s and first flew in 1989.
It cost about $45 billion to develop and build just 21 of those bombers, according to the U.S. General Accounting Office.
The most expensive weapons program ever, Lockheed Martin's F-35 Joint Strike Fighter, is as much as $160 billion over the original budget and a dozen years after Lockheed won the contract the initial jets are not yet deployable in combat.
As a result of such fiascos, Gulick said there's been a shift in Air Force procurement thinking that now emphasizes cost as a driving factor, as well as the need to keep technological requirements in check.
"We need to minimize new development and allow integration of mature technologies and proven existing systems," he said. "That will reduce risk."
The new bomber is expected to combine Stealth technologies from the B-2 bomber and the advanced electronic warfare sensors of the F-22 jet fighter.
Boeing was a major subcontractor to Northrop Grumman on the B-2 and was a partner with Lockheed on the F-22.
Dennis Muilenburg, chief executive of Boeing's defense division, said the two companies can "reduce development risk by leveraging mature technologies and integrating existing systems."
The avoidance of risk is what's behind the shift in thinking from 2006, when the Air Force wanted a new bomber that could be either manned or unmanned depending on the mission.
"The first aircraft will be designed for manned flight only when it comes out," said Gulick. "As time progresses, we'll complete everything to make it unmanned."
"It's better to get something fielded and upgrade it later, rather than hold everything up," Gulick said. "Let's make an initial aircraft buy, keep it simple, get it built."
Technology that Boeing developed for its Phantom Ray-a stealth strike drone about the size of a small jet fighter aircraft-could potentially be scaled up for a bomber program.
It's likely Northrop, which designed the B-2 and whose unmanned stealth drone beat out Boeing's prototype for a Navy contract in 2007, will also compete for the bomber contract.
"We're assuming it will be a competition," said Boeing's Blecher.