We determined the nearly complete mitochondrial genomes of the Arctic Calanus glacialis and its North Atlantic sibling Calanus finmarchicus, which are key zooplankton components in marine ecosystems. The sequenced part of C. glacialis mitogenome is 27,342 bp long and consists of two contigs, while for C. finmarchicus it is 29,462 bp and six contigs, what makes them the longest reported copepod mitogenomes. The typical set of metazoan mitochondrial genes is present in these mitogenomes, although the non-coding regions (NCRs) are unusually long and complex. The mitogenomes of the closest species C. glacialis and C. finmarchicus, followed by the North Pacific C. sinicus, are structurally similar and differ from the much more typical of deep-water, Arctic C. hyperboreus. This evolutionary trend for the expansion of NCRs within the Calanus mitogenomes increases mitochondrial DNA density, what resulted in its similar density to the nuclear genome. Given large differences in the length and structure of C. glacialis and C. finmarchicus mitogenomes, we conclude that the species are genetically distinct and thus cannot hybridize. The molecular resources presented here: the mitogenomic and rDNA sequences, and the database of repetitive elements should facilitate the development of genetic markers suitable in pursuing evolutionary research in copepods.