Polymicrobial diseases significantly impact the health of humans and animals but remain understudied in natural systems. We recently described the Pacific Oyster Mortality Syndrome (POMS), a polymicrobial disease that impacts oyster production and is prevalent worldwide. Analysis of POMS-infected oysters on the French North Atlantic coast revealed that the disease involves co-infection with the endemic ostreid herpesvirus 1 (OsHV-1) and virulent bacterial species such asVibrio crassostreae. However, it is unknown whether consistentVibriopopulations are associated with POMS in different regions, howVibriocontribute to POMS, and how they interact with the OsHV-1 virus during pathogenesis. We resolved theVibriopopulation structure in oysters from a Mediterranean ecosystem and investigated their functions in POMS development. We find thatVibrio harveyiandVibrio rotiferianusare the predominant species found in OsHV-1-diseased oysters and show that OsHV-1 is necessary to reproduce the partition of theVibriocommunity observed in the field. By characterizing the interspecific interactions between OsHV-1,V. harveyiandV. rotiferianus, we find that onlyV. harveyisynergizes with OsHV-1. When co-infected, OsHV-1 andV. harveyibehave cooperatively by promoting mutual growth and accelerating oyster death.V. harveyishowed high virulence potential in oysters and dampened host cellular defenses, making oysters a more favorable niche for microbe colonization. We next investigated the interactions underlying the co-occurrence of diverseVibriospecies in diseased oysters. We found thatV. harveyiharbors genes responsible for the biosynthesis and uptake of a key siderophore called vibrioferrin. This important resource promotes the growth ofV. rotiferianus, a cheater that efficiently colonizes oysters during POMS without costly investment in host manipulation nor metabolite sharing. By connecting field-based approaches, laboratory infection assays and functional genomics, we have uncovered a web of interdependencies that shape the structure and function of the POMS pathobiota. We showed that cooperative behaviors contribute to synergy between bacterial and viral co-infecting partners. Additional cheating behaviors further shape the polymicrobial consortium. Controlling such behaviors or countering their effects opens new avenues for mitigating polymicrobial diseases.