Giggs, 33, has announced his retirement from international football and will lead Wales for the last time in the Euro 2008 qualifier against the Czech Republic in Cardiff.
Then the controversial Bellamy, another Cardiff-born star with 45 caps for his country, will take over the mantle from Giggs.
Wales boss John Toshack said: "Craig is something of a character, but I have complete faith in him as Wales' new captain on a permanent basis."
Giggs informed Toshack of his decision to quit last week ahead of the Wrexham friendly with New Zealand, and Toshack added: "I immediately took Craig aside and told him he would be taking over when Ryan had left."
Bellamy had been captain twice before for the games against Slovakia and Cyprus in October when Giggs was injured.
At the time he was still involved in a high-profile Cardiff court case, and Toshack then defended his decision to appoint the Liverpool striker as his skipper.
Since then Bellamy has been involved in the infamous 'golf club' uproar while away with Liverpool at a Portuguese training camp ahead of the Champions League victory in Barcelona in February that earned him a club fine.
Toshack said: "Without a shadow of a doubt he is the right man for the job. He did it very well earlier in the season. He is committed to Wales and I would accept he is very vocal about things.
"But I had no doubt in appointing him captain on a permanent basis when Ryan leaves us."