It arose in a single dog and has survived in canines ever since, with the cancer cells passing between animals when they mate.
A team led by the Wellcome Trust Sanger Institute near Cambridge decoded the DNA of the cancer.
It revealed the "genetic identikit" of an ancient husky-like dog, which first developed the disease.
The animal was of a medium size with a short, straight coat that was coloured grey-brown or black.
"We do not know why this particular individual gave rise to a transmissible cancer," said lead researcher Dr Elizabeth Murchison.
"But it is fascinating to look back in time and reconstruct the identity of this ancient dog, whose genome is still alive today in the cells of the cancer that it spawned."
The cancer studied is extremely rare - one of only two known types of the disease, both in animals, that is sexually transmissible. Known as dog-transmissible cancer, it causes genital tumours.
By decoding the genome of the cancer, and looking at a type of mutation that acts like a "molecular clock", researchers were able to pinpoint its origin to 11,000 years ago.
Remarkably, the cancer has survived, despite accumulating millions of genetic changes.
Rather than dying out with its first host, the cancer spread by "jumping into other dogs", Dr Murchison added.
The research, published in the journal Science, shows the cancer existed in an isolated population of dogs for much of its history.
Then it spread around the world in the last 500 years, perhaps carried by dogs accompanying explorers on sea voyages.
Apart from this one, the only other known transmissible cancer is facial cancer in Tasmanian devils, spread by biting.
"The genome of the transmissible dog cancer will help us to understand the processes that allow cancers to become transmissible," said Prof Sir Mike Stratton, Director of the Sanger Institute.
Most cancers arise when a single cell in the body gains mutations that cause it to divide out of control.
Cancer cells often spread to different parts of the body in a process known as metastasis, but it is very rare for cancer cells to leave the bodies of their original hosts and spread to other individuals.
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