Puan, described as the "grand old lady" of Perth Zoo, was euthanised on Monday due to age-related complications.
Holly Thompson, a primate supervisor at the zoo, said it was hard to end Puan's life on Monday, but noted it was the right and respectful choice.
Puan had 11 babies among a total of 54 descendants scattered around the world, mostly in the United States, Europe, Australia and the jungle of the Indonesian island of Sumatra.
Her genetics count for just under 10 percent of the global captive population.
"It feels quite surreal to have said goodbye, we all know that life isn't infinite, but for some reason Puan has always just seemed to be the one who might prove us wrong", Hart wrote in a eulogy published in the West Australian newspaper.
'But she remained the matriarch, the quiet, dignified lady she had always been'.
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"Apart from being the oldest member of our colony, she was also the founding member of our world renowned breeding program and leaves an incredible legacy", Ms Thompson said. She spent a majority of her life at the zoo and has over 54 descendants living around the world.
According to the WWF (World Wildlife Fund), there are only about 14,600 Sumatran orangutans.
Perth Zoo officials stated that the Malaysian government gave the Sumatran orangutan as a New Year's Eve gift to an Australia zoo in 1968.
"Puan demanded and deserved respect, and she certainly had it from all her keepers over the years", she wrote. She would tap her feet like a little war dance when she wanted something and it wasn't coming quickly enough.
She added that her legacy as a wild-born orangutan will be carried on by her great-grandson Nyaru who is now living in the jungles of Sumatra.
Zookeeper Martina Hart said Puan "went extremely peacefully".