ABSTRACT The complete mitochondrial genome (mitogenome) of Tropilaelaps mercedesae (Acari: Laelapidae), which is a serious ectoparasite of several honeybee species, was sequenced and characterized for its genomic features. The results were then compared with those of other available Dermanyssoidea members and used to reconstruct phylogenetic relationships within Dermanyssoidea. Moreover, the current T. mercedesae mitogenome from South Korea was compared with publicly available data from China to determine suitable genes for a subsequent population‐level study. Peculiarly, the 15,119‐bp long T. mercedesae mitogenome has an 899‐bp‐long control region containing four copies of a repeat unit that are interrupted by non‐repeat sequences. Additionally, T. mercedesae has a new gene arrangement among the Dermanyssoidea species, revealing eight translocated genes, one inverted tRNA block, and one inverted and translocated tRNA. Phylogenetic analyses, which included all available public data, clearly indicated non‐monophyletic Laelapidae to which the current T. mercedesae is included. Comparison of two geographic samples of T. mercedesae evidenced several protein‐coding genes, including nad5 and cytB (the two most variable), which had higher variability than that of cox1 , thus suggesting the potential usefulness of these gene sequences for population genetic studies. Current T. mercedesae mitogenome sequences could provide baseline information for subsequent population‐level studies and phylogenetic inferences at diverse taxonomic levels within Dermanyssoidea.