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Persistent uplift means the Qinghai-Tibet Plateau (QTP) is an ideal natural laboratory to investigate genome evolution and adaptation within highland environments. However, how paleogeographic and paleoclimatic events influence the genome and population of endemic fish species remains unclear. Glyptosternon maculatum is an ancient endemic fish found on the QTP and the only critically endangered species in the Sisoridae family. Here, we found that major transposons in the G. maculatum genome showed episodic bursts, consistent with contemporaneous geological and climatic events during the QTP formation. Notably, histone genes showed significant expansion in the G. maculatum genome, which may be mediated by long interspersed nuclear elements (LINE) repetitive element duplications. Population analysis showed that ancestral G. maculatum populations experienced two significant depressions 2.6 million years ago (Mya) and 10 000 years ago, exhibiting excellent synchronization with Quaternary glaciation and the Younger Dryas, respectively. Thus, we propose that paleogeography and paleoclimate were dominating driving forces for population dynamics in endemic fish on the QTP. Tectonic movements and temperature fluctuation likely destroyed the habitat and disrupted the drainage connectivity among populations. These factors may have caused severe bottlenecks and limited migration among ancestral G. maculatum populations, resulting in the low genetic diversity and endangered status of the species today.