The Twr y Felin hotel features over 100 original art works portraying the local area and a pop-up gallery by graffiti artist Pure Evil.
It is the result of a seven year £7m development to transform the former 19th century windmill in to a luxury hotel.
The graffiti artist’s eight spray-painted portraits feature Welsh film and music icons such as Tom Jones, Shirley Bassey and Anthony Hopkins.
Charles Uzzell Edwards (Pure Evil) said he hoped the pictures captured ‘an essence of Wales with a slightly sinister twist’.
Boost for tourism
The 19-room venue is a sister site to the Roch Castle Hotel and Penrhiw Hotel, both situated in the Pembrokeshire Coast National Park.
Keith Griffiths, architect and owner of the hotel group, said: “After seven years, it’s wonderful to see this historically-significant building finally restored and given a new lease of life as Wales’ first art hotel.
“We hope that the addition of a third unique luxury hotel with a strong sense of history, art and place will help to further invigorate the economy of St Davids and Pembrokeshire as a whole.”
The development has been backed by the Welsh government through its Tourism Investment Support Scheme.
Edwina Hart, minister for economy, science and transport, said: “St Davids not only holds the title of Britain’s smallest city, but could also be considered to be the art capital of Wales.
“With a wealth of art galleries, heritage attractions, inspiring landscapes, and now, the addition of Wales’ first contemporary art hotel, there is great potential to attract visitors from far and wide to experience the area’s creative and unique offering.”