Crassostrea gigas oysters represent a significant global food source,with 4.7 million tons harvested per year. In 2001, the bacteriumVibrioaestuarianus francensisemerged as a pathogen that causes adult oyster mortality in France and Ireland. Its impact on oyster aquaculture has increased in Europe since its reemergence in 2012. To better understand the evolutionary mechanisms leading to the emergence and persistence over time of this pathogen, we conducted a survey of mollusk diseases through national reference laboratories (NRLs) across Europe. We analyzed54 new genomes of Vibrio aestuarianus(Va) isolated from multiple environmental compartments since 2001, in areas with and withoutbivalve mortalities. We used a combination of comparative genomics and population genetics approaches and show thatVa has a classical epidemic population structure from which the pathogenic Va francensis subspecies emerged and clonally expanded.Furthermore, we identified a specific cus-cop-containing island conferring copper resistance to Va francensiswhose acquisition may have favored the emergence of pathogenic lineages adapted and specialized to oysters.