The origin of eukaryotes is intrinsically linked with mitochondria. Mitochondrial evolution is characterized by a gradual process of gene loss and transfer to the nucleus, and thus eukaryotic genome evolution is intimately tied to mitochondrial DNA. Among animals, the widest variation in mitochondrial genome structure occurs in the non-bilaterian phyla (Porifera, Cnidaria, Ctenophora, Placozoa), where one can find one of the largest, most gene-rich animal mitochondrial genomes, as well as the smallest and most gene-impoverished. This variation in gene content is predicted to have consequences for the evolution of protein-coding genes that remain trapped in mitochondrial DNA, which are mediated primarily by two non-adaptive forces: mutation and random genetic drift. In particular, increased mutation rates lead to the loss of mitochondrial genes, which in turn can lead to elevated mutation rates through drift. This positive feedback mechanism, or mitochondrial ratchet, can manifest itself in different ways depending on the population genetic environment in which mitochondrial DNA is evolving. I will highlight key examples from non-bilaterian animals that illustrate the link between mutation, selection and drift in animal mitochondrial DNA, and represent some of the more extreme ends of the mitochondrial ratchet spectrum. Furthermore, my results show how the mitochondrial ratchet can extend its reach into the nuclear genome, influencing the evolution of nuclear-encoded mitochondrial genes.