Expo '75 was held in Okinawa, Japan, at the Ocean Expo Park, where an aquarium centered on marine life was displayed. In 1976, the Okinawa Ocean Expo Aquarium was established as a national park on the site of the venue. The former aquarium was designed by Fumihiko Maki.

The Okinawa Ocean Expo Aquarium and the Okichan Theater started operations with the facilities used at the Expo. At that time, the largest main tank in the aquarium had a water volume of 1,100,000 litres (291,000 US gal), which was the largest in the world.

The Okinawa Ocean Expo Aquarium is one of the first public aquariums in the world that breeds large sharks and rays such as whale sharks and manta rays.

The captivity of manta ray dates back to at least 1978. The first individual was captured by fishermen, entangled in a net, and threaded through a rope into a spiracle, which severely damaged it. Despite its injuries, the aquarium managed to transport it alive to a tank, where it recognized the tank walls, swam to avoid them, and ultimately survived for 4 days. The second manta ray was brought in in 1985, but died on the same day. The third manta ray brought in was the first to be successfully kept for a long period of time, and the third manta ray went until from 1988 to 2000. The longest kept manta ray was a record that the male reef manta ray, which lived in captivity in 1992, lived for about 23 years.

The first attempt of keeping whale sharks in an aquarium was in 1980. Most were obtained from incidental catches in coastal nets set by fishers (none after 2009), but two were strandings. Several of these were already weak from capture or stranding and some were released, but initial survival rates were low. After the initial difficulties in maintaining the species had been resolved, some have survived long-term in captivity. The record for a whale shark in captivity is an individual that, as of 2024, has lived for more than 29 years in the Okinawa Churaumi Aquarium from Okinawa Ocean Expo Aquarium.

At a symposium held in Baltimore in 1985, the Okinawa Ocean Expo Aquarium was rated to have the most advanced breeding technology in the world for long-term rearing. In 1988, the aquarium won the first Koga Award from JAZA in Japan for breeding two generations of whitetip reef sharks.

From the collapse of the bubble economy, as the park lost incoming tourists, it was believed that a new aquarium would help revive the area and celebrate Okinawa's marine tradition. In addition, since the facility was built for a short-term expo, it deteriorated significantly, and a plan to build a new aquarium was proposed.

The Okinawa Ocean Expo Aquarium was closed in August 2002 due to facility deterioration, and the Okinawa Churaumi Aquarium was opened on 1 November 2002, with a new facility designed by Yukifusa Kokuba (1939–2016), an architect from Okinawa.

The number of visitors in the year before the old aquarium closed was about 430,000, but the number of visitors in the year after the opening of the new building increased to 2.75 million. The number of visitors has continued to increase, with the number of visitors reaching 3,784,132 in 2017 and the cumulative number of visitors reaching 50 million in 2019.

The aquarium's facilities also included a dolphin studio and a sea nursery, but due to deterioration of the concrete and other factors, they have been out of use since the end of January 2007 and have all been removed.

Since 2007, Okinawa Churaumi Aquarium has been conducting an annual learning program for elementary schools in Motobu-cho and Nago city, "Environmental Learning from Sea Turtles", which is an educational activity about ecology and the natural environment through the breeding of sea turtles.

In 2012, a general rest area (Churaumi Plaza) opened. Since 2018, the aquarium has opened its offshore research facility to the public by OKINAWA SAKANA CAMPANY.

In 2020, the number of tourists in Okinawa Prefecture decreased significantly due to the COVID-19 pandemic. The aquarium supervised the Sony aquarium , which was held at the Ginza Sony Building every summer until 2019 before the COVID-19 disaster. The fish once displayed at the Sony Aquarium were brought in from the Okinawa Churaumi Aquarium.

In 2023, he was awarded the Koga Award, the highest prize in Japan for rare species breeding, for his research activities in sea turtle breeding on the IUCN Red List and Appendix I of CITES, for his ecological and conservation research through captive breeding of sea turtles and breeding over two generations.

The Okinawa Churashima Foundation has been certified under the "Okinawa Prefecture CO2 Absorption Certification System" for the management of a total of 380 Garcinia subelliptica, Dypsis lutescens, and other trees around the aquarium during the 2023 CO2 absorption certification period.