Some previous studies have suggested that rates of evolution inferred using molecular sequences vary substantially depending on the time frame over which they are measured, whereas a number of other studies have argued against this proposition. We examined this issue by separating positions of primate mitochondrial genomes that are under different levels of selection constraints. Our results revealed an order of magnitude variation in the evolutionary rates at constrained sites (including nonsynonymous sites, D-loop, and RNA) and virtually an identical rate of evolution at synonymous sites, independent of the timescales over which they were estimated. Although the evolutionary rate at nonsynonymous sites obtained using the European (H1 haplogroup) mitogenomes is 9–15 times higher than that estimated using the human–chimpanzee pair, in contrast, the rates at synonymous sites are similar between these comparisons. We also show that the ratio of divergence at nonsynonymous to synonymous sites estimated using intra- and interspecific comparisons vary up to nine times, which corroborates our results independent of calibration times.