General Sir Mike Jackson, one of the most high profile former generals, rebuked Mr Ainsworth during a fringe debate at the Labour Party conference in Brighton.
It came after Mr Ainsworth said the Westminster Government had pushed the military "too hard" in the past, and called on other major allies to do their bit.
Sir Mike said the UK should act "decisively" at a critical time for the campaign during a debate at a Labour conference fringe event.
Mr Ainsworth said the military had been "running hot" when major operations were taking place in both Iraq and Afghanistan.
The minister said: "To keep 12,000 abroad, deployed in operational theatres, was a lot.
"We were pushing people too hard in many ways. It's not sustainable - sustainable for a short period of time but not for a long period."
Referring to reports that the US will ask Britain to increase its forces in Afghanistan as part of a surge to improve security, Mr Ainsworth said: "We can only make a relatively small part of that as the UK. So others have got to step up to the plate."
Sir Mike insisted that the UK did have the capacity to increase troop levels over a short period.
He added: "When so much blood and treasure has already been expended, if this is a decisive year we should act decisively.
"The Secretary of State talked of the difficulties of sustaining such numbers. Indeed over a number of years I would agree. But if this is a critical year then I think we can do more on that time basis, and indeed should if that is what the commanders on the ground believe is required."
"The decision is not one of military capacity. It is a matter of the politics of the situation."
The US commander of Nato's forces in Afghanistan, General Stanley McChrystal, has reportedly asked for 40,000 more troops. However, no formal request has been made for the UK to add to its presence, which is around 9,100.
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