Mitochondria share a common ancestor with the Alphaproteobacteria, but determining their precise origins is challenging due to inherent difficulties in phylogenetically reconstructing ancient evolutionary events. Nonetheless, phylogenetic accuracy improves with more refined tools and expanded taxon sampling. We investigated mitochondrial origins with the benefit of new, deeply branching genome sequences from the ancient and prolific SAR11 clade of Alphaproteobacteria and publicly available alphaproteobacterial and mitochondrial genome sequences. Using the automated phylogenomic pipeline Hal, we systematically studied the effect of taxon sampling and missing data to accommodate small mitochondrial genomes. The evidence supports a common origin of mitochondria and SAR11 as a sister group to the Rickettsiales. The simplest explanation of these data is that mitochondria evolved from a planktonic marine alphaproteobacterial lineage that participated in multiple inter-specific cell colonization events, in some cases yielding parasitic relationships, but in at least one case producing a symbiosis that characterizes modern eukaryotic life.