"Our diplomatic service does not cooperate actively with Occupy Wall Street, yet your diplomatic service interacts directly with [Russian opposition activists] and supports them," Putin said in a roundtable interview at the Kremlin-funded RT television network's new headquarters.
He was responding to a question from an American RT talk show host on RT's English-language channel.
"In my opinion, that's not right," Putin said in Russian about the alleged State Department support of opposition activists, "because the diplomatic services of a country are supposed to establish relations between governments and not delve into their internal political affairs."
The State Department had no immediate comment.
"Any opposition is good, right and helpful" if it acts within the law, Putin said, adding if people were dissatisfied with the laws, they should try to change them in a "democratic way."
When protesters break the law, the government should use legal methods to "put everyone in the legislative field," Putin said.
"This is what's happening both in the United States and Russia," he said. "But when we do that we are criticized, but when the United States does this, it is considered as a norm. These are the so-called double standards."
He did not discuss the current trial of 12 people charged with violence against police and public disorder in a protest May 6, 2012, the day before Putin was sworn in as president a second time -- a case observers in Moscow call one of the largest politically motivated trials in decades.
More than 400 people were detained at the anti-Kremlin protest in Bolotnaya Square, with nearly 30 facing criminal charges.
Other anti-Putin activists planned to march in Moscow Wednesday protesting what they describe as the government's intimidation and repression of dissent.
Their march would be held on Russia Day, a national holiday officially celebrated with concerts and fireworks.
Putin also criticized U.S. history, saying it began with "substantial ethnic cleansing" of native people during the European settling of North America. He also noted how former Secretary of State Colin Powell recounted in his book the difficulties of growing up black in the United States.
In addition, Putin said Soviet leader Josef Stalin, despite being a despot, would have not dropped an atomic bomb like the United States did at the end of World War II.
"We know Stalin now like never before. He was a dictator and a tyrant, but I very much doubt that in the spring of 1945, if he had been in possession of an atomic bomb, he would have used it against Germany," Putin said in remarks quoted by The Wall Street Journal.
Stalin might have used such a weapon "in 1941-42, when it was a question of life or death" for the Soviet Union, but not later when that was no longer the case.
"But the Americans used it against Japan," he said.
Despite his criticism, he said Moscow and Washington "have united at critical periods in modern history" because of "fundamental interests that unite us."