Marine viral ecology has long been framed by cultivated model systems and a particle-centric view, leaving the diversity of in situ virus-host association poorly resolved. Here, we combined a two-year monthly time series of size-fractionated metagenomes and metatranscriptomes with long-read sequencing and metagenomic Hi-C in the coastal South China Sea. This framework recovered 440,641 species-level viral operational taxonomic units spanning DNA and RNA virospheres. Major viral groups showed contrasting phylogenetic structures, ranging from globally interspersed dsDNA lineages to regionally radiated ssDNA and RNA viruses. Joint abundance and transcriptional profiling across free-living and cellular fractions revealed a continuum of viral lifestyles beyond the conventional lytic–lysogenic dichotomy. Several lineages were predominantly cell-associated and transcriptionally active, indicating metabolically active viral reservoirs that may persist without immediate release. Hi-C further resolved 2,299 high-confidence virus–host links, revealing extensive association networks involving both prokaryotic and eukaryotic viruses and hosts. Temporal tracking of linked pairs showed that, although many viral peaks followed host blooms, a substantial fraction displayed context-dependent trajectories decoupled from contemporaneous host abundance. Together, these non-canonical virus-host associations support a cell-centric view of marine viral ecology in which diverse persistence strategies and broad host associations shape microbial community dynamics.

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