Igor Korobov, 62, had headed the defence ministry's Main Intelligence Directorate (GRU) since 2016 and was the target of US sanctions.
He died on Wednesday after a "long and serious illness," the ministry said.
Korobov's 57-year-old first deputy, Vice Admiral Igor Kostyukov, has been appointed acting GRU chief and is likely become his successor, state news agency TASS said, citing a military source.
Defence Minister Sergei Shoigu expressed his condolences.
"The dear memory of this great man, a faithful Russian son and a patriot of the Motherland... will remain forever in our hearts," the defence ministry said in a statement.
The West has accused the powerful agency of carrying out a number of attacks on foreign soil, including the poisoning of former Russian spy Sergei Skripal and his daughter Yulia with a Soviet-designed nerve agent in Britain in March.
Washington has said the GRU was directly involved in interfering in the 2016 US election through "cyber-enabled activities", while the Netherlands has said they had thwarted a GRU attack on the OPCW global chemical weapons watchdog.
Russia has denied the charges.
First seaman as chief?
Korobov did not participate in a gala marking the centenary of the service in early November when Russian President Vladimir Putin heaped praise on the GRU.
Korobov's first deputy Kostyukov, who is thought to be in charge of Russia's Syria operations at the GRU, reportedly presided over the ceremony.
"If he is appointed, then he will be the first naval seaman in the history of the GRU to become a military intelligence chief," TASS quoted its source as saying.
Korobov, who joined military intelligence in 1985, received the Hero of Russia decoration for his service.
Independent military analyst Pavel Felgenhauer described Korobov as an "intellectual" who spoke several foreign languages.
He was hard-pressed to say whether his successor would usher in any changes, saying the GRU reported to Chief of General Staff Valery Gerasimov, Shoigu and Putin.
"It looks like there are no any major changes on the horizon," he told AFP.
Korobov's predecessor, Igor Sergun, died unexpectedly in January 2016. Some reports said he was killed in Lebanon while on a mission.
Many analysts have derided the GRU for a series of recent blunders including the attack on the Skripals in Salisbury that also killed a British woman and poisoned her partner.
London identified the suspected attackers as GRU agents. After Putin publicly urged them to appear on television, they told state-funded RT channel they travelled to the British city as tourists to admire its famous cathedral.
The same month Korobov was reportedly summoned by Putin and felt unwell afterwards.
'Professionalism and bravery'
But at the November gala, Putin praised the agency's "unique capabilities," saying Russian military spies helped turn around the war in Syria.
"I am sure of your professionalism, personal bravery and decisiveness. That each of you will do everything for Russia and our people," he told the GRU staff.
The GRU is one of Moscow's three spy agencies, along with the SVR foreign intelligence agency and the FSB security service.
Established in 1918, the GRU was considered a rival to the KGB in the Soviet era.
It has an extensive spy network abroad and its highly trained "spetsnaz" special forces have fought in various conflicts, including in Afghanistan and Chechnya. It is also believed to be active in Ukraine and elsewhere.
Very little is known about the agency. Its structure, staff numbers and finances are a state secret. Its emblem is a black bat flying above a globe.
Several top GRU agents have defected to the West.
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via Defense News
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