Cyanobacteria of the genera Synechococcus and Prochlorococcus are the numerically dominant primary producers in the oceans and contribute significantly to global primary production. They are infected by a number of different virus (phage) families, including T7-like cyanophages. Based on DNA polymerase gene phylogeny two discrete T7-like lineages, clade A and B, can be discerned. Phages from clade B encode the psbA photosystem II gene, whereas phages from clade A do not. In order to begin understanding the impact these cyanophages have on cyanobacterial mortality, we developed a culture-independent method for the identification and quantification of T7-like cyanophages based on the solid-phase single molecule polony amplification method. Using this method we found that clade B phages were at least an order of magnitude more abundant than clade A phages in Red Sea surface samples collected during the spring and autumn. Sequencing of selected polonies showed high diversity of clade B phages. These findings suggest that cyanophages carrying the psbA gene are more successful in the Red Sea. The polony method has enabled us to determine, for the first time, differential distributions and abundances of discrete lineages of phages that infect a particular host taxon and greatly improves on current culture-dependent methods.