Irek Ilgiz Hamidullin - believed to be about 55 - faces 12 charges including the attempted murder of a US citizen.
He was seized in 2009 after an attack on Afghan border police and US forces. He was held for five years at Bagram air base before being sent to the US.
He is the first military detainee to be brought to the US from Afghanistan.
Mr Hamidullin, shackled and heavily guarded by federal agents, appeared in a federal court in Richmond, Virginia, on Tuesday.
According to a 19-page indictment, Mr Hamidullin served as an officer in the Soviet army during the war in Afghanistan in the 1970s-80s.
He then stayed in Afghanistan and later joined the Taliban.
The indictment says he commanded three groups of insurgents that attacked the Afghan police and US forces at Camp Leyza, Khost province, in 2009.
He is believed to have directed insurgents armed with anti-aircraft machine guns to fire at US military helicopters responding to the initial attack. The defendant also reportedly used a machine gun to shoot at US troops.
Mr Hamidullin said little during his initial appearance. The next court session is scheduled for Friday.
He was one of 13 foreigners held by the US authorities in Afghanistan.
Washington plans to transfer all the remaining detainees by the end of December, when the US-led Nato combat mission ends.

Two other children, aged 10 and seven, suffered minor injuries in the crash, in Ballards Road, off Church Lane, in Dagenham at 15:50 BST on Friday.
The 22-year-old motorcyclist  was taken to hospital where he later died.
Police said a KTM motorcycle was involved in a collision with a Vauxhall Zafira car. The 38-year-old male driver of the car was not injured.
A post-mortem examination is due to be carried out.
The boy, who was a rear passenger in the car, was taken to an east London hospital where he remains in a serious condition.
No arrests have been made and police are appealing for witnesses.
Anyone with information is asked to call the Serious Collision Investigation Unit based at Chadwell Heath.

Carlsen sealed victory following three weeks of play and a series of tiebreakers in New York.
Karjakin tied against Carlsen in 12 regular rounds but was beaten in the final phase of four quickfire games.
Organisers said the event was followed by about six million chess fans around the world.
Hundreds of spectators paid between $100 and $500 to watch the games at a former fish market in Manhattan, separated from the two grandmasters by soundproof glass.
After his victory, Carlsen's supporters greeted him by cheering and singing "Happy Birthday", to mark his 26th birthday.
The boy who conquered the chess world
The prize of $1.1m (Â£879,000) is divided between the two players with the winner taking 60%.
Chess reached the height of its popularity in the 1970s, when the game was overshadowed by Cold War rivalry.
In 1972, the victory of American Bobby Fischer over Russian defender Boris Spassky at the World Chess Championship in Iceland was dubbed the "match of the century".
Commentators mentioned current geopolitical tensions in connection with this year's match when Kirsan Ilyumzhinov, the Russian president of the World Chess Federation, was accused by the US of collaborating with the Syrian government and barred from travelling to New York.
A former Russian army officer who is alleged to have fought for the Taliban in Afghanistan has appeared in court in the United States on terrorism charges.
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A motorcyclist died and a five-year-old boy was left in a serious condition in a crash in east London.
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Magnus Carlsen of Norway has won the World Chess Championship for the third consecutive time after defeating challenger Sergey Karjakin of Russia.