Wild silkmoths (Saturniidae) are one of the most emblematic and most studied families of moths. Yet, the absence of a robust phylogenetic framework based on a comprehensive taxonomic sampling impedes our understanding of their evolutionary history. We sequenced and analyzed 1,024 ultraconserved elements (UCEs) and their flanking regions to infer the relationships among 338 species of Saturniidae representing all described subfamilies, tribes, and genera. We investigated systematic biases in genomic data and performed dating and historical biogeographic analyses using extinction free and state-speciation and extinction models to document the evolutionary history of wild silkmoths in space and time. Using Gene Genealogy Interrogation, we showed that saturation of nucleotide sequence data blurred our understanding of early divergences and first biogeographic events. Our results support a Neotropical origin of saturniids, but remain undecisive with respect to the extent of the ancestral range for the family. The “traditional” hypothesis of an origin restricted to the Neotropics is supported by models that account for founder-effect dispersal, but a new alternative scenario recovered from other models is proposed and considered a better fit to the hypothetical modes of diversification in these moths. It estimates a broader ancestral range covering the Neotropical, West Nearctic and East Palearctic bioregions and emphasizes the critical role of Beringia as a route between the New World and the Old World during the Eocene. Early branching lineages of Saturniidae all exhibit a very strong geographic conservatism, except for one noticeable exception, the Saturniinae subfamily, that is now present on all continents but Antarctica. Overall, our results provide a framework for in-depth investigations into the spatial and temporal dynamics of all saturniid lineages and for the integration of their evolutionary history into further global studies of biodiversity and conservation. Rather unexpectedly for a taxonomically well-known family such as Saturniidae, the proper alignment of taxonomic divisions and ranks with our phylogenetic results leads us to propose substantial rearrangements of the family classification, including the description of one new subfamily and two new tribes.