Marine cyanobacteria Prochlorococcus and Synechococcus and their viruses (cyanophages) drive global biogeochemical cycles through complex host-virus dynamics. However, current studies on host-virus interactions are trammeled by the limitations of data volume and calculation methods. In this work, we unravel key mechanisms of their coevolution across three fronts. 
First, genomic analysis of phage-resistant mutants revealed that cyanobacteria deploy extracellular defense (e.g., LPS/O-antigen biosynthesis gene mutations blocking phage adsorption) against specialist podoviruses and intracellular strategies (e.g., energy metabolism/DNA replication machinery alterations) against generalist myoviruses. Machine learning identified high-impact resistance genes like PMM1246 (LPS biosynthesis) in Prochlorococcus MED4 and RS11835 (CHAT protease) in Synechococcus WH7803. 
Second, we analyzed 71 cyanophages exhibiting three diel infection traits worldwide: N- trait (no dark adsorption/replication), A-trait (dark adsorption only), and B-trait (burst in the dark). Global metagenomics showed N/A-traits dominate sunlit surface waters, while B-traits peak in deeper dim zones (75–250 m), correlating with environmental factors and host abundance. 
Third, systematic screening uncovered 22,411 group I introns across bacterial/viral genomes. The ancestral introns predominated in ancient phyla like Cyanobacteriota and Bacillota, widely distributed in metabolic genes (e.g., RNR, TnpB) and prophage genes. Phage-host intron sharing was ubiquitous (r = 0.93, p < 9.75e-09), implicating viruses as key vectors for intron dispersal. 
Collectively, this work deciphers how genomic adaptations—from resistance hotspots to diel rhythms and mobile introns—structure marine host-virus networks and ecosystem function.