Nuclear-mitochondrial sequences (NUMTs) can be especially powerful tools for evolutionary studies by providing a window into the nature of ancestral mitochondrial (mt) lineages. Here, we illustrate this property of NUMTs through a survey of such sequences in two species of the jumping bristletail genus Mesomachilis. An ∼1,800 basepair fragment encompassing three mt genes--COI, tRNA-Leu, and COII--was cloned twice for a sample of specimens, and colonies were screened. NUMTs in this genus are abundant and genetically diverse (up to 23% different from the associated mt sequence). Numerous independent nuclear integration events are scattered at different time depths, suggesting a continuous process of NUMT generation. By combining phylogenetic reconstruction with analyses of the pattern of nucleotide substitution on mt and NUMT branches, we inferred the dynamics of NUMT origin and evolution. The majority of NUMTs in the data set have apparently evolved from source mt lineages that were substantially different from the currently associated mt sequence, indicating NUMT transfer via matings among divergent lineages. The original source mt lineages either were unsampled or are extinct. Translocations of NUMTs to new nuclear genomes can preserve NUMTs following extinction of their ancestral mt lineages and can be used to detect mixing between divergent mt lineages and past levels of mt diversity.