Economic cooperation was at the top of Putin's agenda, specifically the completion of a rail link along the North-South Transport Corridor that runs through Iran and Azerbaijan and connects Russia to India.
But bilateral talks between Russia and Iran on Syria and regional security issues also took centre stage.
Photos published online showed Putin holding talks with President Hassan Rouhani and the country's Supreme Leader Ayatollah Ali Khamenei.
On Wednesday, the head of Russia's state-controlled oil giant Rosneft also signed a road map with the National Iranian Oil Company (NIOC) to build joint oil and gas projects worth $30bn.
At any other time, a meeting between leaders of Iran and Russia would be routine diplomacy. However, in a de facto post-ISIL Syria - and Iraq - and with Iran's expanding influence in the region, talks between Moscow and Tehran are likely to shape future events in the region.
"The Russians have now come to realise that if they have a true partner in this part of the world, it is Iran," said Mostafa Khosh Cheshm, a political analyst based in Tehran.
With Iran's support, the Russian foray into Syria has been a battlefield success. Critics had feared it would be an Afghanistan-like quagmire, but instead, it allowed Russia to reposition itself diplomatically and at relatively little cost. Russian casualties have remained in the dozens, despite Moscow's multi-year involvement in the war.
"Russia has revived its lost role," Khosh Cheshm said. "Once it was the former Soviet Union. It decomposed, it collapsed, and it lost everything. Now it's back on the stage. It's rising as a regional power that is soon going to be one of the world powers again."
For Iran, having an ally that is much more influential in world equations is of infinite strategic value. Especially an ally it feels it can trust.
President Hassan Rouhani had publicly positioned the 2015 nuclear agreement as a new beginning with the United States. But the devolution of that deal at the hands of President Donald Trump has pushed Iran even closer to Russia.
"[Iranian leaders] have come to realise they need to pick up Russia and China as their strategic partners," Khosh Cheshm said. "The same approach was in place with President [Mahmoud] Ahmadinejad."
|Both Russia and Iran are involved in the Astana talks aimed at resolving Syria's civil war [AFP]|
Cooperation in the Syrian conflict established trust between the governments and people of Russia and Iran.
"In foreign policy, we never have everlasting friends and everlasting enemies [but] Iran and Russia are developing their strategic ties, and I believe they are in their spring," Khosh Cheshm said. "There is much time left to their winter. They're just at the beginning."
The day before Putin's visit, a Russian company broke ground on two new power plants due to be built at the Bushehr nuclear facility. The project is expected to take 10 years.
The two countries are also dominating the outcome of the Astana talks. A framework for peace in post-war Syria will no doubt take the shape Russia and Iran say it should.
But as the victors of the war, what are their plans for Syria's people?
Davoud Hermidas Bavand was born in 1934 and has spent his entire career as a diplomat. He also served as a member of Iran's delegation to the United Nations.
He says the humanitarian conditions in Syria are a tragedy that cannot be condoned.
"I think that Syria turned out to be the victim of rivalry between three powers in the Middle East; Saudi Arabia, Turkey and Iran," Bavand said. "But bad or good, it has happened already. So the only way is to try to [come] together to pick up Syria and return refugees to Syria."
Bavand said too much blood had been spilled for President Bashar al-Assad to remain in power. And, although his removal would have seemed inconceivable a year ago, Iranian leaders may be more amenable to the idea now.
Without the Islamic State of Iraq and the Levant (ISIL, also known as ISIS) to fill a power vacuum, Bavand said it might be easier to make a quiet change at the top and focus on the welfare of the Syrian people.
"Now the reality is that constructive negotiations continue for a new government and a free election under the auspices of the United Nations," Bavand said.
"Ipso facto, Bashar al-Assad would be removed from the position of power and we hope the new government or coalition could be stable enough to maintain peace and security in Syria and the people would be able to return to their hometowns."
Source: Al Jazeera News