Bakhretdin Khakimov, believed to be in his 60s and known as Sheikh Abdullah after converting to Islam, died of carbon monoxide poisoning from a leaking heater in the western city of Herat, local officials confirmed to AFP.
A representative from Herat's forensics office said there were no suspicious circumstances surrounding his death.
Taliban spokesman Zabihullah Mujahid also confirmed his passing and said he had been taken prisoner after coming to Afghanistan with Soviet forces, before converting to Islam and getting married.
About two million Afghans are thought to have died during the Soviet Union's decade-long involvement in Afghanistan, during which they tried to support an allied communist government.
An international coalition of countries sent arms to anti-Soviet insurgents known as the mujahideen, wearing down Soviet forces who suffered at least 15,000 losses.
Historians say Russia's eventual withdrawal and the subsequent political fallout hastened the collapse of the Soviet Union.
Abdullah was a military intelligence officer and was injured in a 1985 battle, he told AFP in 2015.
He said he owed his life to his Afghan enemies, who found him and treated him.
“I feel very ashamed because I damaged this country, caused losses to people,” he said at the time.
“I stayed in Afghanistan because Afghans are very kind and hospitable people.”
He later worked as a healer and at a museum in Herat, which contains exhibitions about the Soviet invasion of 1979 and the Afghan resistance.
The Soviet withdrawal also precipitated the civil war that gave way to the rise to the Taliban, which ruled the country from 1996 to 2001.
The US withdrawal from Afghanistan last year paved the way for a Taliban comeback, with the hardline group staging a brutal takeover in August 2021, after the precipitous exit of western forces.