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The bacterial origin of mitochondria from an ancient endosymbiosis is now widely accepted and the mitochondrial ancestor is generally believed to belong to the bacterial subdivision α-proteobacteria. The high fraction of mitochondrial proteins encoded in the nucleus has commonly been explained with a massive transfer of genes from the genome of the ancestral mitochondrion.The aim of this work was to get a better understanding of the mitochondrial origin and evolution by comparative genomics and phylogenetic analyses on mitochondria and α-proteobacteria. To this end, we sequenced the genomes of the intracellular parasites Bartonella henselae and Bartonella quintana, the causative agents of cat-scratch disease and trench fever, and compared them with other α-proteobacteria as well as mitochondrial eukaryotes. Our results suggest that the adaptation to an intracellular life-style is coupled to an increased rate of genome degradation and a reduced ability to accommodate environmental changes. Reconstruction of the α-proteobacterial ancestor and phylogenetic analyses of the mitochondrial proteome in yeast revealed that only a small fraction of the proteins used for mitochondrial functions could be traced to the α-proteobacteria. Furthermore, a substantial fraction of the mitochondrial proteins was of eukaryotic origin and while most of the genes of the α-proteobacterial ancestor have been lost, many of those that have been transferred to the nuclear genome seem to encode non-mitochondrial proteins.