The closure of the park was marked by a final show by its two orcas, Wikie and Keijo who were received with rapturous applause by crowds who came for its last day of operations.
Attendance had fallen sharply in recent years but many visitors and employees alike expressed their dismay.
"Our hearts are in pieces," said Salome Mathis, a young keeper who came to say goodbye to her former colleagues at the water park.
The two orcas -- also known as killer whales -- themselves face an uncertain future.
Animal activists had been angered by Marineland's plans to transfer its two killer whales to Japan, a move France's ecology minister said she opposed over Tokyo's more lax animal welfare laws.
The future of the 4,000 other animals of 150 different species including dolphins, sea lions, turtles and fish also remains unclear.
Marineland was hit by a firestorm of controversy in March after two of its orcas died within five months of each other.
The park, near Antibes on the French Riviera, has some 4,000 animals from 150 different species. But visitor numbers have dropped from 1.2 million a year in its heyday when it was a flagship attraction of the Cote d'Azur, to just 425,000 over the last decade.
It employed 103 permanent staff and some 500 seasonal workers.
"I understand that it's closing with the drop in attendance, but I'm disappointed because we could have evolved differently," said Jeremy Lo Vasco, 34, a keeper for ten years.
"For the moment, we're not thinking about our own fate because our priority is that the animals are well, but the hammer blow will come later," he added.
He evoked a "snowball effect" from numerous factors including the floods of 2015 which submerged the site, the 2013 documentary film "Blackfish" denouncing the captivity of cetaceans and the Covid pandemic.
- 'Relocate all animals' -
These led the park's owner, the Spanish group Parques Reunidos, to announce its definitive closure with only recreational activities to be kept during the summer season.
The park has said 90 percent of its visitors come for its orca and dolphin performances.
The closure of Marineland puts an end to a story that began when Count Roland Paulze d'Ivoy de La Poype -- a hero of World War II -- opened the park entirely dedicated to marine fauna based on what he had seen in the United States.
Marineland has until December 2026 to part with its two remaining killer whales Keijo and Wikie.
The priority is to "relocate all of the animals to the best facilities currently available", the park has said.
But the planned move of its last two orcas -- both born in captivity -- to Japan is unacceptable, France's Ecology Minister Agnes Pannier-Runacher told Franceinfo radio in November.
"In Japan, there is not extensive regulation concerning animal welfare," she argued.
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