General Hossein Hamedani was killed on Thursday night while advising the Syrian army on their battle against Islamic State
Hamedani was head of an IRGC unit in charge of security in Tehran, where police, the Guards and its Basij militia allies clashed with protesters. Since 2011, Hamedani has been subjected to international sanctions for violating human rights.
An Iranian official said Hamedani was a close ally of the head of the Quds Force, which is an overseas arm of the IRGC.
"Hamedani was a very influential figure and very close to (Qassem) Soleimani. He was an expert of Syria. A very valuable commander and a true believer of Islam and the (1979 Islamic) revolution (of Iran)," the official said on condition of anonymity.
Tehran denies having any military forces in Syria, but says it has offered "military advice" to Assad's forces in their fight against "terrorist groups". Another Iranian Guards commander was killed in Syria in June.
Iranian news websites have published pictures of Soleimani on the front lines in Iraq helping Iraqi forces fight against IS. Regional sources also told Reuters that Soleimani travelled to Russia in July to plan for the Russian military intervention that has reshaped the Syrian war.
In the biggest deployment of Iranian forces yet, sources told Reuters last week that hundreds of troops had arrived since late September to take part in a major ground offensive planned in west and north-west Syria.
Esmail Kosari, an Iranian politician, said Hamedani helped co-ordination between Syrian armed forces and the voluntary forces in their fight against Isil.
"For years, Hamedani played a very important role in Syria as an adviser ... he played an important role in preventing the fall of Damascus. Then he returned home at the end of his assignment," Mr Kosari told the semi-official Tasnim news agency.
"He returned to Syria for a few days because of his deep knowledge about the area ... and he was martyred in Syria."
Tasnim said that Hamedani's body will be returned to Iran "tonight or tomorrow morning".
The United States and its allies have been waging a year-long air campaign against Isil in Syria, while pushing to diplomatically edge Assad from power.