Despite the global oceanic distribution and recognized biogeochemical impact of coccolithoviruses (EhV), their diversity and genomic potential remain poorly understood. Here we employed a newly developed combination of DNA separation methodologies with next generation sequencing to study the occurrence and progression of natural EhV community genomic variability during an Emiliania huxleyi bloom. The analysis of EhV metagenomes from the early and late stages of an induced bloom led to three main discoveries. Firstly, the observation of resilient and specific genomic signatures in the EhV community associated with the Norwegian coast, which differentiate them from the EhVs isolated in the English Channel (E.C.), and reinforce the existence of limitations to the capacity of dispersal and genomic exchange among EhV populations. Secondly, we report the intriguing finding of a hyper-variable region (approximately 21 kbp in length) in the coccolithovirus genome. Its ecological and evolutionary significance remains to be understood. Thirdly, we observed a clear trend for EhV relative amino-acid diversity to reduce from early to late stages of the bloom. In summary, this study not only validated two new methodological combinations, but proved very useful in the discovery of new genomic features associated with EhV natural communities.