Opossums of the genus Didelphis comprise six species representing the largest American marsupials. Although the monophyly of the species of the genus, as well as that of the genus itself, is well supported in most phylogenetic studies, the relationships among those species are not yet understood. In this study, we present the complete mitochondrial genomes assembled from next‐generation sequencing data for all six Didelphis species and for an outgroup, Lutreolina crassicaudata. Based on this data set, we inferred a highly supported and completely resolved phylogeny of the genus, showing that in the white‐eared opossum group, Didelphis albiventris is the sister taxon to a clade consisting of Didelphis pernigra and Didelphis imperfecta. This resolved phylogeny was used to investigate the evolution of continuous skull traits used in previous taxonomic studies of the genus. Although the first principal component (PC1) based on those traits presents phylogenetic signal, most of the individual traits exhibit no significant information. In general, inference of ancestral states suggested that mean size of individual traits increased in larger species and decreased in smaller species. A congruent pattern was observed for the PC1, which reflected the overall skull size, corroborating previous studies that suggest that variation observed in individual skull characters may be related to skull size. However, traitgrams indicate that variation in overall size in the genus might be related to adaptive evolution.