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The other four finalists were The National Gallery and V&A East Storehouse, both in London, Norwich Castle Museum and Art Gallery, and Cambridge's Fitzwilliam Museum, with each one set to receive £20,000.
June Sarpong OBE, broadcaster and judge for the awards, said what had stood out with The Box was "the sense of pride and connection it has created across Plymouth".
She said: "It is a museum that genuinely belongs to the people it serves.
"Through exhibitions that uncover overlooked histories to welcoming spaces for learning and creativity, The Box is reimagining what being a museum can mean."
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