Abstract Viral infections are major modulators of marine microbial community assembly and biogeochemical cycling. In coral reefs, viral lysis controls bacterial overgrowth that is detrimental to coral health. However, methodological limitations have prevented the identification of viral hosts and quantification of their interaction frequencies. Here, we reconstructed an abundance-resolved virus-bacteria interaction network in the oligotrophic coral reef waters of Curaçao by integrating direct microscopy counts with virus-host links obtained from proximity-ligation, prophage integration, and CRISPR spacers. This network of 3,013 individual links (97 unique species-level interactions) revealed that the abundance of free viral particles was weakly related to host abundance and viral production, as indicated by the cell-associated virus-to-host ratio. The viruses with the highest free and cell-associated virus-to-host ratio, interpreted here as highly productive viruses, formed links with intermediate-to-low abundance hosts belonging to Gammaproteobacteria, Bacteroidia, and Planctomycetia. In contrast, low-production viruses interacted with abundant members of Alphaproteobacteria and Gammaproteobacteria enriched in prophages. These findings highlight the decoupling between viral abundance and production and identify potentially active viruses. We propose that differential decay rates and burst sizes may explain the decoupling between free viral abundance and production and that lysogenic infections play an important role in the ecology of high-abundance hosts.