Prior to becoming prime minister, Fradkov's most prominent post was head of Russia's "tax police", whose job was to put an end to massive tax evasion in Russia.
He was then appointed Russia's representative to the European Union.
The agency Fradkov will head, the Foreign Intelligence Service, is one of the successor agencies to the Soviet-era KGB.
Fradkov's predecessor in the position was Sergei Lebedev, who was appointed executive secretary of the Commonwealth of Independent States, a grouping of 12 former Soviet states, on Friday.
Putin, himself a former KGB officer, pledged in July to strengthen Russia's military capability and to step up spying abroad in response to US policies.
At the time, he singled out the Foreign Intelligence Service in particular to take a more active role in foreign espionage.
Last month, the US complained that Russia, along with China, was spying on the US nearly as much as it did during the Cold War.