Two new Welsh Assembly Government offices in north and mid Wales will house more than 1,000 staff, including more than 300 moved out of Cardiff.
The seafront is one of Aberystwyth's leading attractions
The announcement by minister Sue Essex on Wednesday is the latest stage in a plan to spread civil servants' jobs more widely throughout Wales.
About 525 people will work at a new office in Llandudno Junction, among them 130 posts from Cardiff.
Aberystwyth will host some 500 staff, including 179 from the capital.
It has also been revealed which departments will be housed at each new office.
Among those in Llandudno Junction will be staff from economic development and transport, and parts of education and finance.
Aberystwyth will be home to environment, planning and countryside, and the information age strategy, Cymru ar-Lein.
Ms Essex, who looks after finance, local government and public services, said: "The relocation of a mixture of executive and policy functions on this scale will provide a major boost for the local economies of mid and north Wales."
Both offices will also have what the assembly government called a "first-stop shop" for the public to visit.
Ms Essex said it would bring assembly government "policy and services closer to the people we serve".
The assembly government said it was working "in close partnership" with staff and trade unions and Ms Essex hope employees would move with their work.
A total of 750 civil service jobs will move from Cardiff over the next three years.
It is hoped that the Llandudno Junction office will open in autumn 2007, with Aberystwyth following in 2008.