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The quirky mechanical sheep that emerges from the balcony of the gallery every hour before opening up to reveal a red eyed wolf was commissioned in 1999 as part of the Millennium celebrations.
It has taken pride of place above Lichfield Street since it was installed by artist Andy Plant in spring 2000 - but in recent years it has been broken.
Now 'Baa-bara', as she has affectionately been nicknamed, has been fixed thanks to an art gallery fundraising initiative.
A group of former Northicote School pupils - called the '55ers because they are the Class of 1955 - who meet in the gallery café each month have been at the forefront of the campaign, with donations also being made through the Friends of Wolverhampton Art Gallery.
Councillor John Reynolds, Cabinet Member for City Economy, said: "The public support for the restoration of 'Baa-bara' has been overwhelming.
"She is obviously a much loved feature of the art gallery and it's brilliant to have her up and working again.
"On behalf of the gallery, I would like to thank all those who have contributed to the campaign."
Gillian Burton, one of the '55ers, added: "I often stood across the road from the gallery to catch the bus and marvelled at 'Baa-bara'.
"I'm delighted everyone's fundraising efforts have come to fruition and she is working again.
"It is a great sight and, with the children now breaking up for the summer holidays, I would recommend paying a visit to the gallery to see it."
The piece was inspired by the role Wolverhampton played in the wool trade, which is represented in the crest of the old borough.
The wolf acts as a counterpoint and as well as being the nickname of the city's football team, ties in with the old saying 'a wolf in sheep's clothing'.
Tom Jenkins, Friends of Wolverhampton Art Gallery chairman, said: "The Wolf in Sheep's Clothing is an iconic sculpture which represents an image of the city the city's football fans relate to.
"It puts smiles on people's faces and, besides having a serious edge, art should do that - it is fantastic to see it up and running again."
To see the Wolf in Sheep's Clothing in action watch the video below.
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- released: Monday 20 July, 2015