Viruses of marine cyanobacteria frequently contain auxiliary metabolic genes (AMGs) that augment host metabolism during infection, but little is known about their adaptive significance. We analyzed the distribution and genomic context of 33 AMGs across 60 cyanomyovirus genomes. Similarity in AMG content among cyanomyoviruses was only weakly correlated with phylogenetic relatedness; however, AMG content was generally conserved within the same operational taxonomic unit (OTU). A virus' AMG repertoire was also correlated with its isolation host and environment (coastal versus open ocean). A new analytical method based on shared co-linear blocks revealed that variation in the genomic location of an AMG was negatively correlated with its frequency across the genomes. We propose that rare AMGs are more frequently gained or lost as a result of fluctuating selection pressures, whereas common AMGs are associated with stable selection pressures. Finally, we describe a unique cyanomyovirus (S-CAM7) that lacks many AMGs including the photosynthesis gene psbA.