The monophyletic status of the genus Oreina as well as its phylogenetic relation to the closely related genera Chrysolina, Crosita and Cyrtonus has been debated for several decades. To assess the status of the genus and understand its evolutionary history, we performed a museomics study on 148 museum specimens belonging to 25 of the 28 described Oreina species as well as 19 other chrysomelid species, mainly from the genus Chrysolina. Using innovative molecular methods relying on hyRAD hybridization capture, we succeeded in recovering 2235 shared nuclear loci. Phylogenomic analyses clearly demonstrated that Oreina species form a clade separated from Chrysolina. These analyses also revealed the position of Chrysolina fastuosa outside of the genus Chrysolina, supporting the following taxonomic status updates: Fasta stat. rev., Fasta fastuosa comb. nov. Within the genus Oreina, we further propose the synonymization of Oreina (Frigidorina) syn. n. and Oreina (Virgulatorina) syn. n. with Oreina (Chrysochloa). Divergence time and ancestral range estimations suggested that Oreina originated approximately 53 Ma in the Alps. Ancestral host plant reconstruction revealed key shifts during Oreina diversification. Overall, our study reinforces the importance of museum collections for molecular analysis and the effectiveness of hybridization capture approaches for conducting phylogenomic studies and finely investigating controversial taxonomic debates.