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ABSTRACT Eastern oyster ( Crassostrea virginica ) larvae undergo rapid microbial colonization during early development, a process that may influence larval growth, performance, and hatchery production outcomes. However, the sources and assembly mechanisms of larval-associated bacterial communities remain poorly understood, limiting evidence-based strategies for managing beneficial microbiomes in hatchery settings. We characterized bacterial community composition in 5-day post-fertilization C. virginica larvae and across hatchery water treatment stages using 16S rRNA gene V3-V4 amplicon sequencing. Larval microbiomes were statistically distinct from all sampled water sources (PERMANOVA q ≤ 0.030 ), exhibited 1.9-fold lower Shannon diversity, and showed no relationship to sequential water treatment steps, which themselves did not differ in bacterial composition (all pairwise q = 0.107 ). We identified 39 core bacterial genera present in ≥70% of larval samples, collectively representing 90% of larval sequences and dominated by Rhodobacteraceae/Paracoccaceae (39.5% abundance) and Alteromonadaceae/Marinomonadaceae (24.1%). Critically, 46.2% of core larval sequences belonged to genera highly abundant in larvae but rare (< 0.01%) in all water sources, indicating selective recruitment rather than passive environmental acquisition. Core larval microbiome composition closely parallels that of other marine invertebrates, suggesting conserved host-associated enrichment patterns during early life stages. These results indicate that host-mediated selection dominates larval oyster microbiome assembly, with implications for hatchery management strategies focused on promoting beneficial microbial functions and targeted community supplementation to support consistent larval growth and production efficiency. IMPORTANCE Eastern oysters generate over $200 million annually in U.S. aquaculture and provide critical ecosystem services including water filtration and coastal habitat formation. Successful hatchery production depends not only on preventing disease and mortality, but also on promoting consistent larval growth, development, and yield. Microbial colonization during early larval stages is increasingly recognized as an important contributor to these outcomes, yet the origins and assembly of beneficial larval microbiomes remain poorly understood. Here, we show that oyster larvae do not simply reflect the microbial composition of hatchery water, but instead actively select a consistent set of bacterial partners in early development. This core larval microbiome is dominated by bacterial families associated with antimicrobial activity, nutrient provisioning, and host growth in other marine systems. Notably, these same bacterial families occur in the larvae of distantly related marine invertebrates, suggesting conserved and potentially beneficial host-microbe associations. Our findings indicate that hatchery water treatment alone is unlikely to determine larval microbiome composition. Instead, targeted strategies that promote or supplement beneficial larval-associated bacteria during early development may provide a more effective path toward improving growth, performance, stability, and overall production efficiency in oyster hatcheries.