The landmark building in Bruton, Somerset, is among dozens of sites listed on the register, which identifies Grade I and II*-listed buildings that are under threat from either development pressures, neglect or decay.
The National Trust is working with South Somerset District Council on the restoration project to try to make the dovecote a major tourist attraction and boost Bruton's economy.
Pathways and disabled access to the site have already been upgraded. Trees have been planted and more benches for the area planned. Car parking is to be improved at the Park Wall road area.
Scaffolding was placed round the building three months ago and it is hoped that repointing work on the building's walls with special lime mortar will be completed by the autumn.
There are also plans to set up an interpretation board with a map explaining the Dovecote, the local wildlife and encouraging people to visit the town and museum at the Abbey Park entrance near the railway station.
And there are plans to enhance the area with public art if the town council agrees, and if both funding and planning permissions allow. A Bruton artist has come up with a proposal for a statue depicting a ring of dancers at the site.
Funding for the restoration work has come from the National Trust which manages it, Bruton Town Council, Viridor, Somerset County Council and SSDC.
It is not known why the 16th-century dovecote was built but experts believe it may have been part of Bruton Priory and then used by the Berkeley family as a prospect tower.