In the species-rich Phylum Arthropoda, the mitochondrial genome is relatively well conserved both in terms of number and order of genes. However, specific clades have a 'typical' gene order that differs from the putative arthropod ancestral arrangement. The aim of this work was to compare the rate of mitochondrial gene rearrangements at inter- and intra-taxonomic levels in the Arthropoda and to postulate the most parsimonious ancestral orders representing the four major arthropod lineages. For this purpose, we performed a comparative genomic analysis of arthropod mitochondrial genomes available in the NCBI database. Using a combination of bioinformatics methods that examined mitochondrial gene rearrangements in 464 species of arthropods from three subphyla (Chelicerata, Myriapoda, and Crustacea [except Hexapoda, previously analyzed]), we observed differences in the rate of rearrangement within major lineages. A higher rate of mitochondrial genome rearrangement was observed in Crustacea and Chelicerata compared to Myriapoda. Likewise, early branching clades exhibit less variability in mitochondrial genome order than late branching clades, within each subphylum. We identified 'hot regions' in the mitochondrial genome of each studied subphylum, and postulated the most likely ancestral gene order in each subphylum and taxonomic order. Our work provides new evidence on the evolutionary dynamics of mitochondrial genome gene order in arthropods and new mitochondrial genome architectures in different taxonomic divisions within each major lineage of arthropods.