The US government points to the existence of an armed conflict as the legal underpinning of practices such as indefinite detention of the global militant group's members and allies. Johnson's remarks could ignite a global political debate with arguments from both the left and the right.
The speech to the Oxford Union did not forecast when such a moment would arrive because, it said, al Qaeda and its affiliates in Yemen and elsewhere remain a danger. But Johnson tried to frame the discussion with what he called conventional legal principles rather than a new legal structure emerging from the September 11 attacks.
"Now that efforts by the US military against al Qaeda are in their 12th year, we must also ask ourselves: how will this conflict end?" said Johnson, an appointee of US President Barack Obama. Johnson has been mentioned as a possible US attorney general to succeed Eric Holder in Obama's second term. A former New York corporate lawyer and federal prosecutor, he has been at the centre of internal administration debates on national security since he arrived at the Pentagon as general counsel in 2009.
An "open end" to the conflict has been a defining feature of what then-President George W Bush called a war on terror beginning with the September 11 attacks that destroyed New York's World Trade Centre, damaged the Pentagon and killed 3,000 people. Three days after the attacks, Congress authorised force against all "nations, organisations or persons" who planned them or who aided the planners.
'TIPPING POINT' In courtrooms, congressional hearings and executive orders, US officials with rare exceptions speak of a conflict with no obvious end point. "I think one day they will be defeated, but it's not going to happen any time soon," Senator Lindsey Graham, a Republican, told The Huffington Post website this week.
US Defence Secretary Leon Panetta, Johnson's boss, said in a November 20 speech that US forces had decimated al Qaeda's core and made progress in Yemen and Somalia but needed to avert militant gains in Mali and Nigeria. By asking how the conflict would end, Johnson could provoke a public conversation that gets more specific.
"There will come a tipping point," he said in the speech, "a tipping point at which so many of the leaders and operatives of al Qaeda and its affiliates have been killed or captured, and the group is no longer able to attempt or launch a strategic attack against the United States," that al Qaeda will be "effectively destroyed."
"At that point, we must be able to say to ourselves that our efforts should no longer be considered an 'armed conflict' against al Qaeda and its associated forces." Under that scenario, law enforcement and intelligence agents would go on pursuing individual militants or groups with the military in a reserve role.
"'War' must be regarded as a finite, extraordinary and unnatural state of affairs," Johnson said. "We must not accept the current conflict and all that it entails, as the 'new normal.' Peace must be regarded as the norm toward which the human race continually strives." But what to do with detainees not charged with crimes - such as some of those held at the Guantanamo Bay US Naval Base in Cuba - might still be a slow process, Johnson said. In one of 25 footnotes to the written remarks, Johnson cited a US Supreme Court ruling from 1948 that allowed the detention of German nationals for six years after fighting with Germany ended.