A central goal of population genomics is to unveil the evolutionary forces driving genomic divergence. Although genomic islands have been extensively studied in angiosperms, the patterns of genomic divergence remain poorly understood in gymnosperms. Here, by re-sequencing the whole genome of 130 individuals of Welwitschia mirabilis, we reveal significant genomic differentiation among its geographically close populations. Population genomic analyses suggest that geographical isolation and species characteristics play important roles in triggering and maintaining population divergence. We also identify multiple genomic islands of elevated divergence, which are primarily attributed to divergent sorting of ancient polymorphisms and divergence hitchhiking. Further genome-wide association analyses indicate that Welwitschia has an XY-type sex-determination system, with the sex-linked region located at 72.04–92.82 Mb on chromosome 6. Our findings are important for comprehending the evolutionary forces shaping genomic patterns of differentiation and the genetic basis of sex determination in gymnosperms. Keywords: population genomics, geographical isolation, genomic islands, sex-linked region, Gnetales, gymnosperm.