The excretory and osmoregulatory organs (nephridia) of lumbricid earthworms are densely colonized by extracellular bacterial symbionts belonging to the newly established betaproteobacterial genus Verminephrobacter. The nephridial symbiont of the earthworm Eisenia fetida was subjected to full genome sequencing along with two of its closest relatives; the plant pathogenic Acidovorax avena subsp. citrulli and the free-living Acidovorax sp. JS42. In addition, the genome of the nephridial symbiont of the earthworm Aporrectodea tuberculata was partially sequenced. In order to resolve the functional and evolutionary basis of the symbiosis we annotated and compared the genomes. The genomes ranged in size from 4.4 to 5.6 Mbp, the E. fetida symbiont genome being the largest. The symbiont genomes showed no evidence of gene-loss related to any particular type of functional gene category. In contrast, genes predicted to be involved in transport processes were highly overrepresented in the symbiont genomes due to massive paralogous expansion of genes encoding ABC-type amino acid and peptide uptake systems. Thus, symbionts seem well-adapted to the nephridial environment being able to profit from proteinaceous excretion products. Gene order was highly conserved between the genomes of Acidovorax avena and Acidovorax sp. JS42, whereas the E. fetida symbiont genome held very little conservation of gene order compared to either of the latter two. Repetitive sequences were excessively abundant throughout the genomes of both symbionts. Together, this is indicative of high recombinatorial frequency in the symbiont genomes the function of which is presently poorly understood.