The plans for a museum were put on hold as the threat of war rose (and as it subsequently broke out).

In the summer of 1949 the first exhibition was set up in the Drommedaris, the 16th century defensive tower in the harbour; this marked the birth of the indoor part of the museum.

Due to the success of this exhibition, the Zuiderzeemuseum obtained warehouses on the Wierdijk (including the Peperhuis) from seed company Sluis & Groot [nl] for the symbolic amount of 1 guilder.

It consists of a string of (original and replicated) 17th century buildings of which some were used by the VOC and contains both temporary exhibitions as well permanent installations.

The indoor museum also displays artifacts from other aspects of the Zuiderzee cultural past, including paintings, furniture and traditional, locally-worn costumes ('klederdracht').

A large variety of buildings are on display in the outdoor museum: wind mill, lime kilns, fish-smoking house, steam laundry, drugstore, pharmacy, basketmaker, blacksmith, cheese warehouse, school, and hairdresser's, amongst others.

Some aspects of local Zuiderzee history are also on display, especially during the period from April to November with typical old Dutch activities, like old games and building clog boats, and demonstrations of ancient crafts such as rope-making, cooperage, basket making and herring smoking.