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The United States will also have to deal with troublesome partners like Pakistan, whose unmatched ability to play both sides of a fight frustrated generations of American leaders.

William J. Burns, the agency’s director, has said that it is ready to collect intelligence and conduct operations from afar, or “over the horizon,” but he told lawmakers in the spring that operatives’ ability to gather intelligence and act on threats will erode. “That’s simply a fact,” said Mr. Burns, who traveled to Kabul this week for secret talks with the Taliban.

Challenges for the C.I.A. lie ahead in Afghanistan, the senior intelligence official acknowledged, while adding that the agency was not starting from scratch. It had long predicted the collapse of the Afghan government and a Taliban victory, and since at least July had warned that they could come sooner than expected.

In the days after the Sept. 11 attacks, C.I.A. officers were the first to meet with Afghan militia fighters. The agency went on to notch successes in Afghanistan, ruthlessly hunting and killing Qaeda operatives, its primary mission in the country after Sept. 11.

It built a vast network of informants who met their agency handlers in Afghanistan, then used the information to conduct drone strikes against suspected terrorists. The agency prevented Al Qaeda from using Afghanistan as a base to mount a large-scale attack against the United States as it had on Sept. 11.

But that chapter came with a cost in both life and reputation. At least 19 personnel have been killed in Afghanistan — a death toll eclipsed only by the agency’s losses during the Vietnam War. Several agency paramilitary operatives would later die fighting the Islamic State, a sign of how far afield the original mission had strayed. The last C.I.A. operative to die in Afghanistan was a former elite reconnaissance Marine, killed in a firefight in May 2019, a grim bookend to the conflict.