Earlier, the two presidents attended a summit of heads of countries in the Caspian Sea area.
Iran's nuclear programme is topping the agenda, with the BBC's Jon Leyne in Tehran saying Iran is seeking Russian help in fending off new UN sanctions.
The visit went ahead despite Kremlin warnings of an assassination threat.
The alleged plot to kill the Russian president prompted Mr Putin's staff to cast doubt on the trip, only for the president to announce that he was not deterred.
The Iranian government played down the threat.
Iran's refusal to end uranium enrichment has led to the US and other Western countries pressing for a new round of UN sanctions.
Washington is convinced that Tehran is pursuing nuclear weapons - a charge Iran denies - and has refused to rule out the use of force to resolve the issue.
At the meeting of the five states bordering the Caspian Sea - Russia, Iran, Azerbaijan, Kazakhstan and Turkmenistan - the countries' leaders signed a declaration agreeing to never allow their territory to be used for an attack on another littoral state.
"The parties emphasise that in no circumstances will they allow their territory to be used by a third country to commit aggression or other military action against one of the parties," AFP news agency quoted the text as saying.
Mr Putin used the meeting to warn against any military attack on Iran and to support its right to nuclear energy.
He told a press conference after the meeting that the five countries had "expressed the idea that peaceful nuclear activities must be allowed".
"Russia is the only country helping Iran to construct a nuclear power station for peaceful ends," he added, in reference to Iran's still unfinished first nuclear energy plant in Bushehr.
As well as meeting President Ahmadinejad, Mr Putin will hold talks with Iran's powerful spiritual leader, Ayatollah Ali Khamenei.
Building plan
Our correspondent in Tehran says that the talks are crucial for the Iranians. Until now Moscow has been blocking any new UN sanctions, saying it wants to enable the UN's nuclear watchdog, the IAEA, to work with Iran on clearing up outstanding issues.
As well as wanting to secure diplomatic help in preventing sanctions, Iran also wants to ensure continued Russian technical assistance.
The government hopes Mr Putin will confirm that Moscow will complete the Bushehr nuclear reactor being built by Russian engineers.
The programme has been dogged by delays, with Moscow saying Tehran is behind with its payments and Iran accusing Russia of dragging its feet for political reasons, our correspondent says.
It is not clear quite how much support Mr Putin is prepared to give Iran in its showdown with the West.
Mr Putin will certainly be calling for more flexibility from the Iranian government over the nuclear issue and no-one should forget the deep legacy of suspicion that exists between Russia and Iran, our correspondent says.
Moscow has called for a peaceful resolution of the dispute, urging the international community to show patience.
"It is futile to frighten Iran and its people - they are not scared," Mr Putin said before the visit.
Suicide bomb threat
Mr Putin travelled to Tehran from Germany where he met Chancellor Angela Merkel for talks somewhat overshadowed by the alleged assassination plot.
Russian media had quoted unnamed security sources as saying suicide bombers and kidnappers were plotting to kill Mr Putin in Tehran.
Mr Putin's spokesman Dmitry Peskov told the BBC that such reports were "very serious".
But the Russian president dismissed the claims, telling reporters: "Of course I am going to Iran.
"If I listened to what the security services said, I would never leave my home."
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