Monk fruit (Siraitia grosvenorii, Cucurbitaceae) is globally renowned for its triterpenoid glycoside mogroside V, a high-intensity, non-caloric natural sweetener. However, its domestication and mogroside biosynthesis remain largely unknown. Here, we report a haplotype-resolved telomere-to-telomere (T2T) gapless genome for monk fruit, consisting of 14 chromosomes with genome sizes of 316.21 Mb (Hap1) and 316.07 Mb (Hap2). Comparative genomic analyses of the haplotypes revealed that structural variations and transposable elements have significantly contributed to genomic variation and architecture in monk fruit. Population genomic analyses based on 173 re-sequenced genomes indicated that cultivated monk fruit was mainly domesticated in situ from local wild populations in northern Guangxi of China, and that it likely experienced a mild domestication bottleneck, while exhibiting low genetic diversity. Demographic inference further revealed that the low genetic diversity is largely attributed to demographic changes driven by historical climate shifts. Selective sweeps were identified across all chromosomes of cultivated monk fruit, among which are genes exhibiting diverse putative functions and involved in various biosynthetic processes and secondary metabolism. This pattern of selective sweeps demonstrates the joint role of artificial selection and demographic changes in shaping the genomic landscape of cultivated monk fruit. Furthermore, comparative transcriptome analyses showed a pronounced temporally specific expression pattern among mogroside biosynthesis genes during fruit development and delineated additional candidate genes potentially involved in mogroside biosynthesis. This study not only provides insights into the domestication and mogroside biosynthesis of monk fruit but also lays a valuable genomic foundation for its molecular breeding and mogroside-targeted synthetic biology.

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