The toad-headed agama (genus Phrynocephalus) is a widely distributed group of lizards across Central Eurasia, inhabiting diverse arid and semi-arid environments from the Caspian Basin to the Qinghai-Tibetan Plateau (QTP). Despite considerable research efforts over the past decades, a robust phylogenetic framework for Phrynocephalus has remained elusive. In this study, we collected 26 samples representing a substantial proportion of the distribution area of this genus and established a well-supported phylogeny based on whole-genome sequencing and phylogenomic approaches. We found that the Phrynocephalus lizards comprised three major clades, including the Western Asia, the Central Asia and the viviparous clades. Furthermore, we provided compelling evidence for an ancient hybridization event that led to the speciation of P. mystaceus, which likely contributed to the observed phylogenetic discordance across the genome. Divergence time estimation and ancestral area reconstruction indicated that Phrynocephalus lizards originated approximately 39.72 million years ago in the Central Asia and Iranian Plateau region, followed by successive Miocene dispersals into the QTP, Gobi Desert, and Arabian Peninsula. Our results illuminate how hybridization and historical range dynamics have jointly driven the origin and diversification of Phrynocephalus, providing new insights into the formation of biodiversity in Eurasia.