The 70ft (21m) finback arrived at Cambridge University's Zoology department 150 years ago, after washing up dead on a Sussex beach.
It was taken down from display when the Museum of Zoology closed in 2013 for a Â£4m makeover.
Re-assembling and re-hanging the whale took two people about four weeks.
The finback (Balaeonoptera physalus) - the second largest species after the blue whale - is thought to have weighed about 80 tonnes, the equivalent of eight double-decker buses, when it was alive.
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It washed up in Pevensey Bay on 14 November, 1865, after a storm.
The mammal was sold at auction for Â£38 to 10 local fisherman who cut it up under the guidance of William Henry Flower, conservator of the Museum of the Royal College of Surgeons.
Mr Flower told Cambridge University about the "magnificent skeleton", and the department bought it, finally putting it on public display 30 years later.
For years it took centre-stage, dwarfing the museum's four million other specimens, including the skeleton of a Dodo and many animals collected by naturalist Charles Darwin.
However, it was consigned to storage boxes for three years until being put back together and re-hung in a new glass display area.
Putting it back together took "a lot of patience, a lot of effort and a lot of labour", collections manager Matt Lowe said.
"It's really iconic, it's 150 years old - exactly the same age as the museum itself," he added.
Whale-watchers will be able to appreciate the whale's sheer scale when the museum reopens to the public next summer.
A giant whale skeleton dismantled and put into storage for three years during a museum refurbishment has been put back together, bone by bone.