Its strong intergenerational bottlenecks and effectively asexual reproduction have led Buchnera aphidicola, the endocellular symbiotic bacterium of aphids, to spectacular evolutionary and genomic changes in comparison with its free-living bacterial cousins. These changes summarize into high fixation rates of mildly deleterious destabilizing mutations. This predicts a sharp decline of its fitness and the consequent early demise of this endosymbiotic bacterium. Its survival for hundreds of millions of years casts doubt on genetic drift as the sole evolutionary force and seeks further explanation. We identify in Buchnera selection to increase the robustness of proteins to misfolding translation errors. Translational robustness varies between Buchnera lineages and protein functional categories. Metabolic proteins have been under selection for translational efficiency, whereas evolutionary rates of proteins involved in fundamental cellular processes have been largely determined by selection for translational robustness. We detect the strongest signal of translational robustness in B. aphidicola Cinara cedri with a very similar pattern to that inferred for the most common symbiotic ancestor of Buchnera lineages. This indicates that B. aphidicola Cinara cedri lineage may have probably reached the minimum evolutionary stable gene composition for endosymbiotic lifestyle. The evolutionary patterns from the comparative genomic analyses of these endosymbionts support a paradoxically complex dynamic for apparently simple genomes.