One of the most striking features of modern chemosynthesis-based ecosystems surrounding methane seeps is the presence of abundant chemosymbiotic bivalves. However, such accumulations have rarely been reported from Palaeozoic to mid-Mesozoic seeps, and it is widely thought that general trends in the evolution of chemosynthetic communities paralleled those typifying most marine environments, with the bivalve prevalence starting in the Mesozoic and with Palaeozoic seeps being dominated by brachiopods. Here, we report a discovery of bivalve clusters in the oldest-known methane seep that hosted metazoan fauna, dated to the late Silurian. We identify the bivalves, externally very similar to modern chemosymbiotic forms, as members of the extinct family Modiomorphidae, known previously from a younger, Devonian seep. The bivalves inhabited the seep at a stage of increased fluid flow, when they co-occurred with atrypid brachiopods, and display a set of morphological characteristics suggesting a seep-obligate lifestyle. We conclude that bivalves colonised chemosynthesis-based ecosystems at least as early as brachiopods and apparently first developed specialized lineages able to thrive in seep-related habitats for a prolonged period of time. Rather than being simple ecological successors of brachiopods, rich bivalve communities represent an ancient and recurring theme in the evolution of chemosynthetic assemblages.