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Mortality events in marine bivalves cause substantial economic losses in aquaculture, yet the microbial dynamics underlying these events remain poorly characterized. Here, we investigated succession patterns in oyster-associated Vibrio communities during mortality events by sampling eastern oysters (<i>Crassostrea virginica</i>) at a North Carolina commercial farm that has experienced repeated, unexplained mortality events. Through whole-genome sequencing of 110 Vibrio isolates from 26 oysters sampled across mortality events in two consecutive years, we identified six conserved phylogenetic clades with distinct temporal associations. <i>Vibrio mediterranei</i> and a clade of resident vibrios consistently dominated the initial cultured community at the onset of mortality. However, <i>V. mediterranei</i> was absent as mortality progressed, coinciding with increased abundance of <i>V. harveyi</i>, <i>V. alginolyticus</i>, <i>V. diabolicus</i>, and <i>V. agarivorans</i>. Comparative genomic analysis revealed that initial isolates were enriched in pathways associated with host colonization and complex carbon metabolism, while isolates from elevated mortality showed enrichment in virulence mechanisms and adaptation to degraded host tissues. Temporal separation between genetically distinct clades suggests microbial competition shapes community assembly during mortality events that ultimately reached >85% mortality in both years. This predictable succession from commensal to potentially pathogenic Vibrio species provides genome-level insight into microbial community dynamics during oyster mortality. The consistent loss of <i>V. mediterranei</i> prior to severe mortality suggests this species could serve as a bioindicator for early warning systems to mitigate economic losses in shellfish aquaculture.IMPORTANCEMortality events in aquaculture systems represent complex host-microbe-environment interactions that challenge our ability to predict and prevent disease. By characterizing succession patterns in oyster-associated Vibrio communities at whole-genome resolution, we reveal a consistent transition from metabolically versatile species associated with healthy oysters to functionally distinct Vibrio taxa enriched in virulence factors and tissue degradation pathways as mortality progresses. This genome-level evidence for predictable community reorganization suggests that monitoring commensal Vibrio populations, particularly the presence or absence of <i>Vibrio mediterranei</i>, could provide earlier warning of impending disease compared to tracking only known pathogens. This shift in monitoring approach could advance aquaculture disease management while expanding our fundamental understanding of how microbial community transitions contribute to host health and disease progression.