The portrait, painted by John Napper in 1952, shows Queen Elizabeth II with an extraordinary long neck.
John Napper himself described it as “a beautiful painting of a queen, but not this Queen”.
After spending six decades in council vaults, the portrait went on display in Liverpool’s St George’s Hall on Friday.
The city’s deputy Lord Mayor, Gary Millar, said: “We are very proud that Liverpool now has the original first painting hanging in St George’s Hall, which has been rehung to celebrate the anniversary of the Queen’s Coronation.
“It will be the first thing people will see if they come to get married or have a civil partnership or attend a citizenship ceremony.
“It is an honor for us to work with the friends of the hall, the staff there and the city council to rehang this beautiful painting.”
John Napper, who died in 2001, painted a second portrait of The Queen, with a smaller neck, after the original was rejected by the council. That picture still hangs in Liverpool Town Hall.
The artist’s widow, Pauline Napper, told the Daily Telegraph: “I remember the painting well. He was disappointed with the angle at which he painted it, he only had one sitting.
“It was due to be hung up high so that you would look at it from below. If you looked at it from that angle it looked normal.
“Then when they showed it they didn’t put it up high and then it didn’t look like the Queen.”
Pauline Napper added: “It is a beautiful painting, obviously he would have been pleased that it is going on display. I am pleased too, it is a beautiful portrait.”
The public unveiling of the work comes a week after the first official portrait of the Duchess of Cambridge was panned by some critics.
Paul Emsley’s work, which hangs in the National Portrait Gallery, was accused of making Kate Middleton look older and lifeless.
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