The CIA has made plans to close its network of secret bases in Afghanistan and pull its personnel back to Kabul this summer.
It is an unexpectedly abrupt withdrawal that the US military fears will deprive it of vital intelligence while thousands of American troops remain in the country, officials said.
CIA director John Brennan informed military commanders in March that his agency would start to shut down Afghan operations outside Kabul, the capital.
It will involve removing CIA clandestine officers and analysts as well as National Security Agency specialists responsible for intercepting insurgents' communications, which have been a rich source of daily intelligence, the officials said.
Pentagon officials warn that the CIA drawdown is coming at a time when insurgent attacks normally intensify, after a winter lull. As a result, the plan has strained relations between the agency and military commanders in Kabul, the officials said.
"They are beginning their own retrograde and they kind of sprung it on the military, which is raising concern," said a senior military official.
Intelligence officials confirmed the drawdown would occur, but said the pace of it was still uncertain and no final plan had been approved.
They linked the move to the steady pullout of US combat troops from America's longest war. Soldiers and marines have provided protection and logistics support for intelligence-gathering outposts, which are often inside US military facilities.
Hundreds of those frontline military bases and camps have now closed, although dozens are still operating.
"The CIA footprint is entirely dependent on the military's," a senior US official said. A former CIA operator who has spoken to current officers about the pullback, said: "There is no stomach in the building for going out there on our own. We are not putting our people out there without US forces."
John Maguire, who retired from the CIA in 2005 after 23 years as a case officer, noted that CIA officers on horseback were the first US forces into Afghanistan after the terrorist attacks of September 11, 2001.
He criticised the spy service for the current drawdown.
"There is ample evidence and a long historical record of the agency working alone in any number of difficult and dangerous places, and if they can't do it by themselves without the military, then they should close the organisation," he said.
The CIA also plans this summer to stop paying the salaries of Afghan paramilitary forces that it has armed and trained for more than a decade to help fight the Taliban-led insurgency in the country's east, near the Pakistani border. It is unclear what will happen to the militias.
The Pentagon is trying to persuade the CIA to slow its withdrawal, arguing that keeping CIA and NSA operators in the field as long as possible would help prevent a surge in militant attacks before the end of the year, when most US troops are due to leave.
About 33,000 US troops remain in Afghanistan, down from a peak of 100,000 in 2011.
Marine Corps General Joseph Dunford Jnr, the top commander in Afghanistan, has offered to help the CIA close its intelligence-gathering installations and remove its equipment late this year.
By taking on that task, he hopes to persuade the CIA to remain in the field until at least October, one of the officials said.
Pentagon officials are also exploring whether the military can take over financial support of the CIA-backed militias to keep the Afghans from leaving the fight or switching sides, officials said.
Some of the frontline units have already have been disbanded, according to a report by news website The Daily Beast.
Brennan told military officials that the CIA would be able to continue gathering intelligence and targeting militants even after pulling back to Kabul and the nearby Bagram air base, one official said.
Brennan told the military that the CIA faced other priorities outside Afghanistan and Pakistan that were compelling it to redeploy staff, the official said.
The agency is increasingly focused on threats in Syria, Yemen and parts of Africa as al-Qaeda has morphed into regional affiliates that are seen as more dangerous to the US and its allies.