© 2023 Royal Entomological Society.Our study focuses on the origin, dispersal patterns, evolutionary strategies and systematics of Poecilimon, the largest bush-cricket genus in the Palaearctic with over 150 taxa described. We employ phylogenetic and divergence time estimation analyses based on multilocus sequence data (ND2 + COI + 12 S + 16 S + ITS+28 S), perform ancestral area reconstruction, and track the evolution of behavioural (evolution of sound communication) and morpho-physiological traits (body size and shape, and spermatophore size) in this genus. Based on our results, we propose a revised systematics of Poecilimon, including description of a new species, P. nivalis sp. n., and hypothesize three stages in the evolution of Poecilimon. (1) In the early evolution of the genus in Tortonian, when open dry habitats appeared in the Eastern Mediterranean, diversification rates were low and speciation was possibly induced by vicariance and habitat fragmentation; physiology and morphology during this period retained their ancestral states but the evolution of main lineages may have been accompanied by behavioural specializations. (2) Climate cooling and aridification during the Messinian induced dispersals and adaptation to new habitats, followed by physiological and behavioural adaptations; major clades formed or started diversifying. (3) Starting at the end of Messinian and continuing through the Plio- and Pleistocene, a few dispersal events from Anatolia to the Balkans took place and climatic oscillations were followed by allo- and parapatric divergence of habitat specialists, while ecological adaptations enhanced song diversity and led to morpho-physiological changes.