General David Petraeus has warned that President Hamid Karzai's latest public criticism of US strategy threatens to undermine progress in the war.
The Afghan leader told the Washington Post there should be fewer US troops, and called for an end to special forces night raids.
Gen Petraeus, the coalition commander in Afghanistan, was said to be astonished by the remarks.
President Karzai has been increasingly outspoken about the Western mission.
He told the Washington Post on Saturday: "The time has come to reduce the presence of, you know, boots in Afghanistan... to reduce the intrusiveness into the daily Afghan life."
Calling for a halt to night raids, he said: "I don't like it in any manner and the Afghan people don't like these raids in any manner."
Expressing "astonishment and disappointment", Gen David Petraeus said such public criticism risked making his own position "untenable", Afghan and US officials told the Washington Post.
Downplaying the Afghan president's comments on Monday, Waheed Omar, Mr Karzai's spokesman, told news agency AP he had not been criticising the overall strategy, and he had confidence in Gen Petraeus.
Mr Karzai may want the US forces to reduce their footprint, but the BBC's Quentin Sommerville in Kabul says the reality is that Afghan forces simply are not ready to take charge.
Our correspondent adds that there is particular anger from the US side over the president's demand to reduce special forces missions.
The night raids, which have increased dramatically in recent months, are a central plank of Gen Petraeus's strategy to target the Taliban.
But many people would agree that the night raids are deeply unpopular, our correspondent says.
He adds Afghans are also angry that the war against the Taliban has not been won, and that foreign troops have the run of the country.
On Friday, Nato's 28 leaders will begin a two-day summit in the Portuguese capital of Lisbon to discuss handing security responsibility to Afghan forces next year.
Nato hopes for a gradual drawdown of foreign troops from the current peak of about 150,000 soldiers from more than 40 countries.