He quit as deputy prime minister amid denials from the Kremlin that the step was connected to a row over the alleged embezzlement of state funds.
Mr Surkov had criticised an inquiry into a project he had been supervising.
He was once thought to be one of Russia's most powerful men, creating its system of "managed democracy".
But in December 2011, he was removed from his job as deputy head of the presidential administration.
That was soon after elections overshadowed by allegations of ballot-rigging and the biggest street protests in Moscow since Soviet times.
Mr Surkov was appointed deputy prime minister instead, first under President Dmitry Medvedev, then under Mr Putin when he returned to the Kremlin last year.
'Puppet master'Put in charge of modernising the Russian economy, he publicly clashed with investigators last week over allegations of fraud against an official at the Skolkovo innovation hub, outside Moscow. He warned them against prejudicing the inquiry.
However, presidential spokesman Dmitry Peskov suggested Mr Surkov had resigned after Mr Putin criticised ministers for failing to carry out his orders.
In a Kremlin career spanning 12 years, Mr Surkov saw through controversial political reforms which cemented the grip of Mr Putin and his allies on power.
When Russian tycoon Mikhail Prokhorov pulled out of the 2011 parliamentary election campaign, he famously blamed him, saying: "There is a puppet master in this country who long ago privatised the political system... His name is Vladislav Yurevich Surkov."
Mr Surkov, 48, told Russia's Kommersant newspaper on Wednesday he would explain his reason for resigning at the "appropriate" time.
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