B chromosomes are supernumerary chromosomes found in the karyotypes of approximately 15% of all eukaryotic species. They present parasitic behavior and do not follow the standard Mendelian pattern of inheritance, resulting in an imbalance in gametogenesis. The evolutionary dynamics of B chromosomes is still unknown for many species, but studies indicate that the accumulation of repetitive sequences plays an important role in the differentiation of these elements. We analyzed morphology, frequency, and possible homologies amongst different B chromosomes found in an isolated Akodon montensis population in southern Brazil. Repetitive sequences (18S, 5S rDNA and telomeric sequences) were used to test for their accumulation on the supernumerary chromosomes and describe their localization in the species. The results indicate 4 different B chromosome morphotypes, and DNA libraries were generated for 3 of them. 18S rDNA was labelled polymorphically, except in the B chromosomes, whereas the 5S rDNA was located exclusively in an interstitial position on the long arm of chromosome 5. Chromosome painting with the B probes based on FISH revealed a homologous composition for all B chromosome morphotypes and no homology with the chromosomes in the A complement. B chromosomes found in this population may have a common origin and subsequently diversified in size and morphology.