Natural history collections worldwide house billions of specimens, representing one of the most globally important biobanks. In recent years, the advent of next‐generation sequencing has significantly reduced the challenges of obtaining considerable genetic information from historical museum specimens. Crickets in the Australian tribe Eurepini Robillard are a good example of a taxon in which such museomic data have particularly strong potential to advance systematic knowledge, because comprehensive sampling requires decades of work over a very wide area. The tribe currently comprises 64 described species in five genera. Previous studies conflict in the generic relationships inferred for this tribe, all of which are poorly resolved, being based on limited data and sampling. In addition, there has so far been no systematic research for this tribe with extensive taxon sampling, and therefore, the consequence for genus boundaries remains to be investigated. To investigate phylogenetic relationships within Eurepini, we first applied the genome skimming approach to obtain molecular data from a comprehensive sample of Eurepini museum specimens. Of the 69 specimens sampled representing 61 described species, mainly including holotype specimens, we obtained 50 complete and 11 partially complete mitogenomes. Three nuclear genes (H3, 18S, and 28S) were also partially recovered for nearly all of these specimens. Phylogenetic analyses performed with mitogenomes plus three nuclear genes using maximum likelihood and Bayesian inference generated well‐supported and highly congruent topologies. Eurepini was strongly recovered monophyletic with eight well‐defined groups. These groups are used to revise the systematics of the tribe based on a combination of molecular phylogenetics and morphology. The phylogenetic results support the current definition of three genera (Eurepa Walker, Arilpa Otte & Alexander and Eurepella Otte & Alexander), lead us to redefine three genera (Salmanites Chopard, Napieria Baehr and Piestodactylus Saussure), and define and describe two new genera: Miripella Robillard, Tan & Su gen.nov. and Arrakis Robillard, Tan & Su gen.nov. Our results reinforce the importance of natural history collections as a repository for information on biodiversity and genetics, and provide the first comprehensive and robust phylogenetic framework for future systematic and evolutionary studies of Eurepini.