It holds a staggering 7,500 tonnes of water - roughly equal to three Olympic-sized swimming pools.
Eighty species live in the Kuroshio Sea tank, including yellow-fin tuna, bonito (a type of large mackerel) and manta rays.
But the daddy of them all is the world's biggest fish, the whale shark - which can grow to be 12 metres long and needs a quarter of a tonne of food every week.
Only three aquariums in the world have tanks large enough to house these giant creatures.
The four whale sharks at Churaumi move around comfortably - swimming diagonally past each other and feeding with their long tails touching the plethora of colourful corals at the bottom of the tank.
Rather than hand-pick fish from around the world and force them to mix in unfamiliar waters, the emphasis in the Kuroshio Sea tank is placed on local sea life.
All the species housed here can be found thriving around Okinawa - and even the water itself is pumped in from 300 metres offshore.
It is no surprise, then, that this titanic space requires an equally large observation panel.
The world's largest aquarium window, it measures a staggering 8.2 metres by 22.5 metres and is more than 60cm thick - this is necessary to stop the tank from collapsing under the huge water pressure placed on the glass.
It was constructed from seven acrylic-resin sheets, which were stuck together using a strong glue with a secret formula.
The appearance is dazzling and the window is so clear that each year millions of visitors can believe, for a moment, that they have stepped into a magical underwater world.
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