The ocean plays essential roles in Earth's biochemistry. Most of the nutrient transformations that fuel trophic webs in the ocean are mediated by microorganisms. The extent of phylogenetic and metabolic diversity of key culture and uncultured marine microbial clades started to be revealed due to progress in sequencing technologies, however we still lack a comprehensive understanding of the evolutionary processes that led to the microbial diversity we see in the ocean today. In this dissertation, I apply phylogenomic and comparative genomic methods to explore the evolutionary genomics of bacterial and archaeal clades that are relevant due to their abundance and biogeochemical activities in the ocean. In Chapter 1, I review relevant literature regarding the evolutionary genomics of marine bacteria and archaea, with emphasis on the origins of marine microbial diversity and the evolution of genome architecture. In Chapter 2, I use a comparative framework to get insights into the evolutionary forces driving genome streamlining in the Ca. Marinimicrobia, a clade widely distributed in the ocean. This project shows that differences in the environmental conditions found along the water column led to contrasting mechanisms of evolution and ultimately genome architectures. In Chapter 3, I assess the phylogenetic signal and congruence of marker genes commonly used for phylogenetic studies of bacteria and archaea and propose a pipeline and a set of genes that provide a robust phylogenetic signal for the reconstruction of multi-domain phylogenies. In Chapter 4, I apply a phylogeny-based statistical approach to evaluate how tightly genome size in bacteria and archaea is linked to evolutionary ii history, including marine clades. I present evidence suggesting that phylogenetic history and environmental complexity are strong drivers of genome size in prokaryotes. Lastly, in Chapter 5, I estimate the emergence time of marine bacterial and archaeal clades in the context of the Prokaryotic Tree of Life and demonstrate that the diversification of these groups is linked to the three main oxygenation periods occurring throughout Earth's history. I also identify the metabolic novelties that likely led to the colonization of marine realms. Here I present methodological frameworks in the fields of comparative genomics and phylogenomics to study the evolution of marine microbial diversity and show evidence suggesting that the main evolutionary processes leading to the extant diversity seen in the ocean today are intimately linked to geological and biological innovations occurring throughout Earth's history. / Doctor of Philosophy / The ocean plays essential roles in the functioning of our planet. Many of the nutrient's transformation happening in marine environments are mediated by microorganisms, whose metabolic activities underpin higher trophic levels. The identity of the most prevalent marine microbial groups has been reveled during the last two decades through sequencing technologies. Despite having a great progress in our understanding of the functions that these microorganisms have in the ocean; we still lack information about the evolutionary processes that allowed their diversification and colonization into marine realms. In this work, I developed and applied computational strategies to disentangle the evolutionary genomics of marine microorganisms. One particularity about most these marine groups is that they have very small genomes. To explore the evolutionary forces driving their genome reduction, I analyzed a broad set of genomes of Marinimicrobia, a bacterial group widely distributed in the ocean. This analysis shows that genome reduction in Marinimicrobia is driven by negative selection, an evolutionary force that allows the deletion of non-essential genes, subsequently leading to genome reduction. Moreover, I developed a benchmarked pipeline for the reconstruction of phylogenetic trees to study the evolutionary relationships of microorganisms. This pipeline allowed me to link the diversification of the main marine groups and the geological periods in which they first emerged. I discovered that the colonization of these groups happened during three different periods, which are coincident with the main oxygenation events occurring across Earth's history. Moreover, the diversification of vi marine microbial groups was associated with the acquisition of genes to exploit the newly created niches that followed the oxygenation of the atmosphere and the ocean. Overall, my work shows that the diversification of the marine microbial clades that are essential for the functioning of the ocean is intimately linked to the redox state of the ocean and the atmosphere throughout Earth's history.