Bacteria belonging to the genus Aminobacter are metabolically versatile organisms thriving in both natural and anthropized terrestrial environments. To date, the taxonomy of this genus is poorly defined due to the unavailability of the genomic sequence of A. anthyllidis LMG 26462^T and the presence of unclassified Aminobacter strains. Here, we determined the genome sequence of A. anthyllidis LMG 26462^T and performed phylogenomic, average nucleotide identity and digital DNA-DNA hybridization analyses of 17 members of genus Aminobacter. Our results indicate that 16S rRNA-based phylogeny does not provide sufficient species-level discrimination, since most of the unclassified Aminobacter strains belong to valid Aminobacter species or are putative new species. Since some members of the genus Aminobacter can utilize certain C1 compounds, such as methylamines and methyl halides, a comparative genomic analysis was performed to characterize the genetic basis of some degradative/assimilative pathways in the whole genus. Our findings suggest that all Aminobacter species are heterotrophic methylotrophs able to generate the methylene tetrahydrofolate intermediate through multiple oxidative pathways of C1 compounds and convey it in the serine cycle. Moreover, all Aminobacter species carry genes implicated in the degradation of phosphonates via the C-P lyase pathway, whereas only A. anthyllidis LMG 26462^T contains a symbiosis island implicated in nodulation and nitrogen fixation.