Racing-Metro full-back Andrea Masi scored the only try for the home side and Mirco Bergamasco kicked 17 points as Italy secured their first win in this year's tournament.
France scored tries through Vincent Clerc and Morgan Parra, with the latter kicking three penalties and a conversion.
The Azzurri, who had eight France-based players in their side, punished the French for a sloppy performance at the Stadio Flaminio.
It was the second defeat in succession for Marc Lievremont's side following their 17-9 loss to England at Twickenham, while Italy were finally rewarded for their efforts following defeats to Ireland, England and Wales.
Italy put points on the board after two minutes after being awarded a penalty when France skipper Thierry Dusautoir was caught offside.
Bergamasco converted from close range to bring the stadium to life, but the visitors produced a well-worked try in the 14th minute.
Les Bleus spread the ball wide to Clerc and he chipped it over Gonzalo Canale and dived over to hand France a 5-3 lead. Parra missed the conversion.
France soon came close to scoring their second try but Aurelien Rougerie was brought back for a forward pass.
An excellent scrummage from the French led to Martin Castrogiovanni being called offside. Parra converted the penalty to extend France's lead to 8-3 after 20 minutes.
France were then penalised for being offside at a ruck and Bergamasco converted from close range.
Italy showed attacking flair after the interval with a great run from Luciano Orquera but Italy lost possession when they were threatening.
Italy coach Nick Mallett made a double substitution with Leonardo Ghiraldini on for Carlo Festuccia and Salvatore Perugini coming on for Andrea Lo Cicero. But it was France who extended their lead as Parra converted a penalty to make it 11-6 before the visitors scored the second try of the game in the 50th minute.
Francois Trinh-Duc did well to penetrate Italy's defence and he sent Parra over, the same player converting to put his side 12 points clear.
Italy had the chance to reduce the deficit but Bergamasco missed two penalty kicks before the hour mark.
The home side made amends soon after with Masi scoring the try after Fabio Semenzato darted down the wing and fired the ball out to Masi on the wing.
The try inspired Italy and Bergamasco made no mistake with another penalty only for Parra to respond with a penalty fro France.
With 10 minutes remaining, France conceded their ninth penalty of the match and Bergamasco slotted the ball through the posts to cut the gap to 21-19.
Four minutes later Italy were on top 22-21 after Bergamasco took advantage of another penalty and the home fans roared their side on as Italy held on for an historic win.
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