The museum was founded in 1983 by the Mykonian George M. Drakopoulos and it opened in 1985 with the goal of preserving and promoting the study of Greek maritime history and tradition, in particular the evolution and activities of the merchant ship in the Aegean Sea. Drakopoulos' has been awarded with the Athens Academy Award and with the World Ship Trust's award for Individual Achievement for his work with the museum.

The Aegean Maritime Museum was the first museum in Greece that rescued and restored living historical exhibits to operate as they were originally designed and built: the "Armenistis" lighthouse (built in 1890), the "perama" type sailing ship "Evangelistria" (built in 1940) and the cable-laying ship "Thalis o Milesios" (built in 1909). The "Armenistis" lighthouse operates again in the Museum's garden, in Mykonos, while "Evangelistria" and "Thalis o Milesios" are berthed at the Hellenic Navy's Museum wharf at the Paleo Phaliro (Athens) marina.

There are also replicas of famous historical ships such as the Ancient Egyptian round leather boat, which was reconstructed based on Herodotus’ descriptions and a Hellenistic ship recovered in Cyprus and reconstructed in Perama. Also on display is an impressive collection of ancient coins with nautical scenes from the 5th century BC to the 4th century AD and a variety of elaborate shipping instruments. In the museum's garden are reproductions of ancient marble gravestones from the islands of Mykonos and Delos that depict shipwrecks and sailors who were lost at sea.

The Aegean Maritime Museum participates in international conferences and exhibitions, as well as in the festivities of the Hellenic Navy for the Maritime Week. It is also active in publishing works of the Greek maritime history.