<p>Mitochondrial genomes of some animals remained almost unchanged architecturally for over half a billion of years, while other lineages exhibit conspecific variability. The drivers underlying this disparity remain unknown. We analyse over 10,000 bilaterian mitogenomes to test whether locomotory capacity and parasitic lifestyle can explain the variability in architectural evolutionary rates, and attempt to answer multiple other evolutionary questions. Double-stranded (genes on both strands) architecture is the most likely ancestral state for most major radiations (phylum and above). We identify over twenty transitions to single-stranded architectures, and the evidence of state-reversals (in Annelida and Mollusca). Gene order rearrangement and sequence evolution rates are positively correlated (<i>r</i> = 0.69), and both are increased in single-stranded mitogenomes, parasites, and species with low locomotory capacity. The latter two categories exhibit increased prevalence of single-strandedness and GC skew inversions. Mitogenome size is negatively correlated with evolutionary rates, whereas the effective population size is decoupled from all tested evolutionary variables. Endotherms exhibit slower evolutionary rates than ectotherms in Bilateria, but faster in Chordata. Here, we provide evidence that purifying selection mediated by locomotory capacity and species ecology is a major driver of mitogenomic architectural evolution, but other variables are required to fully explain the observed patterns.</p>