Early lifestages of the Pacific oyster (Crassostrea gigas) are highly susceptible to infection by OsHV-1 μVar, but little information exists regarding metabolic or pathophysiological responses of larval hosts. Using a metabolomics approach, we identified a range of metabolic and immunological responses in oyster larvae exposed to OsHV-1 μVar; some of which have not previously been reported in molluscs. Multivariate analyses of entire metabolite profiles were able to separate infected from non-infected larvae. Correlation analysis revealed the presence of major perturbations in the underlying biochemical networks and secondary pathway analysis of functionally-related metabolites identified a number of prospective pathways differentially regulated in virus-exposed larvae. These results provide new insights into the pathogenic mechanisms of OsHV-1 infection in oyster larvae, which may be applied to develop disease mitigation strategies and/or as new phenotypic information for selective breeding programmes aiming to enhance viral resistance.