Bacteriophages (phages) are the most abundant biological entities in the biosphere and are the dominant "organisms" in marine environments, exerting an enormous influence on marine microbial populations. Metagenomic projects, such as the Global Ocean Sampling expedition (GOS), have demonstrated the predominance of tailed phages (Caudovirales), particularly T4 superfamily cyanophages (Cyano-T4s), in the marine milieu. Whereas previous metagenomic analyses were limited to gene content information, here we present a comparative analysis of over 300 phage scaffolds assembled from the viral fraction of the GOS data. This assembly permits the examination of synteny (organization) of the genes on the scaffolds and their comparison with the genome sequences from cultured Cyano-T4s. We employ comparative genomics and a novel usage of network visualization software to show that the scaffold phylogenies are similar to those of the traditional marker genes they contain. Importantly, these uncultured metagenomic scaffolds quite closely match the organization of the "core genome" of the known Cyano-T4s. This indicates that the current view of genome architecture in the Cyano-T4s is not seriously biased by being based on a small number of cultured phages, and we can be confident that they accurately reflect the diverse population of such viruses in marine surface waters.