Anthropogenic activities have impacted marine ecosystems at extraordinary scales. Biogenic reef ecosystems built by the European flat oyster (Ostrea edulis) typically declined before scientific monitoring. The past form and extent of these habitats thus remains unknown, with such information potentially providing valuable perspectives for current management and policy. Collating >1,600 records published over 350 years, we created a map of historical oyster reef presence at the resolution of 10 km² across its biogeographic range, including documenting abundant reef habitats along the coasts of France, Denmark, Ireland and the United Kingdom. Spatial extent data were available from just 26% of locations yet totalled >1.7 million hectares (median reef size = 29.9 ha, range 0.01–1,536,000 ha), with 190 associated macrofauna species from 13 phyla described. Our analysis demonstrates that oyster reefs were once a dominant three-dimensional feature of European coastlines, with their loss pointing to a fundamental restructuring and ‘flattening’ of coastal and shallow-shelf seafloors. This unique empirical record demonstrates the highly degraded nature of European seas and provides key baseline context for international restoration commitments.