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Topmouth culter (Culter alburnus) is an ecologically and economically important species belonging to the subfamily Culterinae that is native to and widespread in East Asia. Intraspecific variation of semi‐buoyant and adhesive eggs in topmouth culter provides an ideal opportunity to investigate the genetic mechanisms of spawning habits underlying the adaptive radiation of cyprinids in East Asia. In this study, we present a chromosome‐level genome assembly of topmouth culter and re‐sequenced 158 individuals from six locations in China covering three geographical groups and two egg type variations. The topmouth culter genome size was 1.05 Gb, with a contig N50 length of 17.8 Mb and anchored onto 24 chromosomes. Phylogenetic analysis showed that the divergence time of the Culterinae was coinciding with the time of initiation of the Asian monsoon intensification. Gene family evolutionary analysis indicated that the expanded gene families in topmouth culter were associated with dietary adaptation. Population‐level genetic analysis indicated clear differentiation among the six populations, which were clustered into three distinct clusters, consistent with their geographical divergence. The historical effective population size of topmouth culter correlated with the Tibetan Plateau uplifting according to the demographic history reconstruction. A selective sweep analysis between adhesive and semi‐buoyant egg populations revealed the genes associated with the hydration and adhesiveness of eggs, indicating divergent selection towards different hydrological environments. This study offers a high‐resolution genetic resource for further studies on evolutionary adaptation, genetic breeding and conservation of topmouth culter, providing insights into the molecular mechanisms for egg type variation of East Asian cyprinids. [ABSTRACT FROM AUTHOR]