Designed by noted architects George D. Mason and Albert Kahn,[5] it opened on August 18, 1904, and was the oldest continually operating public aquarium in North America when it closed on April 3, 2005.

[6] The 10,000-square-foot (930 m2) historic building features a single large gallery with an arched ceiling covered in green glass tile to evoke an underwater feeling.

[8] The aquarium basement served as a speakeasy during Prohibition[9] and later held large fish which no longer fit the Belle Isle Zoo's gallery tanks.

[13] The Aquarium now operates with free public admission, welcoming visitors Friday-Sunday from 10am - 4pm, thanks to community funding and the efforts of Belle Isle Conservancy.

The aquarium made news in 2002 when one of its female white-spotted bamboo sharks gave birth to two young despite not having been near a male in six years, in a suspected rare case of parthenogenesis.

The Aquarium has a formal partnership with the Michigan Department of Natural Resources to assist with repopulating sturgeon in the Detroit River.