Too many works of art and historical artefacts are hidden from public view, the government has said.
Parry's Portrait of Omai was jointly bought by three UK museums
Arts minister Estelle Morris says major museums in England should allow smaller galleries to exhibit undisplayed items.
She said there was a growing appetite for "serious" culture in the country and called for the "cultural centre of gravity" to move away from London.
Her comments come as a consultation paper on the future of museums in England is published.
"The best of our culture should be accessible to all, no matter where they live," said Ms Morris.
She accepted that several institutions had already begun to address the problem.
The National Portrait Gallery, the Captain Cook Memorial Museum in Whitby, and the National Museums and Galleries of Wales were singled out for praise.
They jointly bought and displayed in turn the Portrait of Omai, Joseph Banks and Dr Daniel Solander - a painting by 18th century British artist William Parry.
Mrs Morris says smaller museums are desperate for new exhibits
But while large parts of major London collections are rarely seen by the public, museums outside the capital are crying out to show fresh items, the former education secretary added.
A spokeswoman for the British Museum told BBC News there were a number of reasons for keeping artefacts in storage.
"Of the others, one million are flints which are of interest to archaeologists and would not be interesting to display. Others are paintings or drawings which cannot be displayed for conservation reasons.
"And there are objects which are part of study collections which are available to view with an appointment."
The British Museum has seven million objects in its collection, of which 75,000 are on display
The National Gallery has 10,500 portraits. Of these 60% are regularly displayed at the National Portrait Gallery or elsewhere
"But everything that is worth seeing is available to the public."
The British Museum also highlighted its new loans programme, Partnership UK, which sees new acquisitions and older artefacts from their collection being displayed at museums around the country.
The first loan, the 4,000-year-old terracotta artwork Queen Of The Night, has already been displayed in Glasgow, Sunderland, Leicester and Cardiff. It is currently at the Birmingham Museums and Art Gallery.
London's National Gallery, which says that 80 per cent of its collection is currently on display, said it welcomed Ms Morris' remarks as it was continuing to build on its own programme of touring exhibitions and loans.
Their latest exhibition, The Stuff Of Life, opened at Bristol City Museum and Art Gallery on 15 January. The display, which includes works by Van Gogh, Cezanne and Chardin, will travel to Newcastle in April before returning to London in the summer.
Ms Morris hopes the consultation paper, Understanding the Future: Museums and 21st Century Life, will initiate a public debate on the subject.