It was established at the Australian National University (ANU) in 1962 as a teaching aid to help students in the Canberra region learn about the ancient Greek and Roman worlds.

[2] The museum has been housed in the foyer of the AD Hope building at the ANU's main campus in Acton since the 1970s.

While the thieves had forced the cabinet open, there was reported to be no evidence that they had broken into the AD Hope building.

[5] A major refurbishment of the museum during 2010 included new display cases, captions and interpretative panels for items as well as improved lighting.

[10] In September 2023, it was discovered that an amphora vase, a fish plate and a Roman marble portrait head were bought by the Museum throughout the 20th century "in good faith", however they were found to have been illegally excavated by its original dealers.