The great majority of microorganisms have yet to be cultured and characterised. This so-called “microbial dark matter” is now being revealed at an ever-increasing rate by sequence-based culture independent methods. In the past few years, thousands of near complete genomes of uncultured microbes have been assembled from sequence data obtained directly from environmental and clinical sources providing the opportunity to fully articulate microbial diversity for the first time. Current estimates suggest that cultured microorganisms only capture ~15% of total microbial diversity based on evolutionary divergence of marker genes. We propose a genome-based taxonomy founded on the existing classification of cultured organisms, but corrected for polyphyletic groups and calibrated to take into account relative evolutionary divergence. The result is a fully systematized classification of Bacteria in an evolutionary framework. Of ~100,000 publicly available bacterial genomes, over half required one or more changes to their existing taxonomy. These include extensive changes at both high ranks, such as amalgamation of the Candidate Phyla Radiation into one phylum and low ranks including subdivision of the genus Clostridium into more than 100 distinct genera.