Some neotropical rodents are of special interest because they are an important source of animal protein for human indigenous populations throughout Latin America. This is the case of the genus Dasyprocta (agouties). However, we still do not know how many species, taxa, or lineages are within Dasyprocta. To address this issue, we analyzed the complete mitogenomes of 93 specimens in addition to three mitochondrial genes of 128 specimens of Dasyprocta belonging to six supposed species (D. fuliginosa, D. punctata, D. leporina, D. kalinowski, D. ruatanica, and D. azarae). The phylogenetic results indicated five different lineages within D. fuliginosa, with two being polyphyletic (one more related to D. leporina and another more related to D. punctata). D. kalinowski, a species endemic to Peru, was un-differentiable from one of these D. fuliginosa lineages. D. azarae was related with some of the lineages of D. fuliginosa. Within D. leporina, two significant lineages were found (in central Atlantic Brazil and on the Caribbean islands of Trinidad and Tobago). Within D. punctata, three lineages were detected, one in Central America (central and northern), including D. ruatanica, a supposed endemic species on Roatan Island, Honduras, another in central and southern Panama, and another in trans-Andean and Pacific Colombia and Ecuador. Some of the lineages of D. fuliginosa from the western Amazon yielded the most ancestral haplotypes (around 7 million years ago, MYA, Late Miocene). In contrast, haplotypes of a lineage of D. punctata and those of a lineage of D. leporina (Trinidad and Tobago) were the most derived (around 0.2–0.3 MYA, Pleistocene). Other population genetic results showed that all groups or lineages presented elevated levels of genetic diversity, with the exception D. leporina in Trinidad and Tobago. Their lower genetic diversity is probably related to founder effect during the colonization of the Caribbean island, due to a bottleneck. Some of these Dasyprocta taxa showed some population expansions during the Pleistocene, but all of the lineages experienced some population decrease during the last 10,000–20,000 years. Note that some lineages showed a small population increase in the last few centuries. The spatial genetic structure was highly developed throughout the Neotropics for Dasyprocta. According to this study, (1) coat color (routinely used in the systematics of this rodent) is not valuable from a phylogenetic and systematics perspective and (2) two supposedly endemic species (D. kalinowski and D. ruatanica) were not full species. These results are of vital importance for the biological conservation of the different taxa and lineages of this rodent.