Puan -- Indonesian for "lady" -- died on Monday at Perth Zoo, where she had lived since being gifted by Malaysia in 1968.
"She did so much for the colony at Perth Zoo and the survival of her species," said primate supervisor Holly Thompson.
"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.
"Her genetics count for just under 10 percent of the global zoological population."
Puan had 11 children and a total of 54 descendants in the United States, Europe, Australasia and the jungles of Sumatra. Her great grandson Nyaru was the latest individual to be released into the wild.
Born in 1956, she was noted by the Guinness Book of Records as being the oldest verified Sumatran orangutan in the world. Female orangutans rarely live beyond 50 in the wild.
Thompson said she was an aloof and independent individual.
"You always knew where you stood with Puan, and she would actually stamp her foot if she was dissatisfied with something you did."
She leaves two daughters at the zoo, along with four grandchildren and a great grandson.