Dermestidae (Bostrichoidea) exploit diverse food sources including fungal mycelia, but notably they as saprophagous, feeding on decomposing and dried flesh and keratin of animals and plants. Some of them live in spider webs, vertebrate and social insect nests, while others cause damage in human dwellings. Here, we use mitogenomics to reconstruct their phylogeny and evolution of life history strategies. We recovered serial splits of Orphilinae, Thorictinae + Dermestinae, Attageninae, Trinodinae and Megatominae, and we dated the origins of all subfamilies between the Middle Jurassic and Upper Cretaceous. Extant genera started their diversification in the Middle Cretaceous, except for Dermestes that originated in the Eocene. Mycetophagy, the likely feeding style of the common ancestor with Endecatomidae, was retained only by Orphilinae. Since the Late Jurassic, most dermestids have been saprophagous with the preference for desiccated tissue. We infer a scenario of feeding preferences from mycetophagy moving to saprophagy, always depending on food with low water content, followed by the shift from cryptic life in crevices and wood, to commensalism with social Hymenoptera, and ultimately feeding on angiosperm pollen as adults. The dependence on spider larders evolved already in the Early Cretaceous, but lineages with this specialized strategy remained species‐poor. We date the origin of exploitation of vertebrate carcasses to the Eocene when modern mammalian fauna became dominant. The diversification of Megatominae (62% of known dermestids) and Attagenus Latreille (17%) coincides with the radiation of angiosperms. Using mitogenomic phylogeny, we analysed relationships among dermestid subfamiles and dated the origins of major groups. The dating analyses estimate the split of Dermestidae and Ptinidae + Bostrichidae to the Middle Triassic and the origins of major genera to the Middle Cretaceous. Mycetophagy predisposes to saprophagy; flightlessness and host specificity drive diversification; free living in crevices precedes commensalism; and association with the angiosperms is important for groups living in arid ecosystems.