Bacteriophages play key roles in microbial evolution, marine nutrient cycling and human disease. Phages are genetically diverse, and their genome architectures are characteristically mosaic, driven by horizontal gene transfer with other phages and host genomes. As a consequence, phage evolution is complex and their genomes are composed of genes with distinct and varied evolutionary histories. However, there are conflicting perspectives on the roles of mosaicism and the extent to which it generates a spectrum of genome diversity or genetically discrete populations. Here, we show that bacteriophages evolve within two general evolutionary modes that differ in the extent of horizontal gene transfer by an order of magnitude. Temperate phages distribute into high and low gene flux modes, whereas lytic phages share only the lower gene flux mode. The evolutionary modes are also a function of the bacterial host and different proportions of temperate and lytic phages are distributed in either mode depending on the host phylum. Groups of genetically related phages fall into either the high or low gene flux modes, suggesting there are genetic as well as ecological drivers of horizontal gene transfer rates. Consequently, genome mosaicism varies depending on the host, lifestyle and genetic constitution of phages.