The Russian president added that the power vacuum following these revolutions led to the rise of terrorist groups in the region — including the Islamic State group.
He told the United Nations General Assembly it would be an "enormous mistake" not to cooperate with the Syrian government to combat the extremist group.
"No one but President (Bashar) Assad's armed forces and Kurdish militia are truly fighting the Islamic State and other terrorist organizations in Syria," he said.
In an earlier speech at the U.N., President Barack Obama said it would be a mistake to think that Syria could be stable under Assad.
Acknowledging some of the criticism lobbed at Russia's proposal, Putin said his country is only proposing to help save the world from terrorism.
Read MoreObama at the UN: I won't hesitate to use force
"I must note that such an honest and frank approach from Russia has been recently used as a pretext to accuse it of its growing ambitions — as if those who say it has no ambitions at all. However, it's not about Russia's ambitions, dear colleagues, but about the recognition of the fact that we can no longer tolerate the current state of affairs in the world," he said.
He proposed a "generally broad international coalition against terrorism," likening the suggestion to the anti-Hitler coalition that brought together disparate interests to battle fascism in Europe.
Putin warned that international policy toward the region has led to an Islamic State with plans that "go further" than simply dominating the Middle East. And citing recent data about failures in successfully recruiting "moderate" Syrian opposition, Putin said countries opposed to Assad are simply worsening the situation.
"We believe that any attempts to play games with terrorists, let alone to arm them, are not just short-sighted, but hazardous. This may result in the global terrorist threat increasing dramatically and engulfing new regions," the Russian leader said.
On the subject of the ongoing civil war in Ukraine, Putin warned that NATO expansion could lead to other similar crises. He called for all sides in the conflict — which he said was sparked by a "military coup" orchestrated "by the outside" — to respect the Minsk agreements, or else risk more violence.