The flowerpot snake (Indotyphlops braminus) is the only known parthenogenetic and triploid species within Serpentes. However, the genetic basis underlying this phenomenon remains unresolved. We investigated the genomic complexities of this rare all-female triploid reptile. On the basis of the newly assembled genome, we revealed 40 chromosomes grouped into three subgenomes (A, B, and C). Comparative genomic analysis with related diploid species revealed a chromosome fusion event in ancestral genomes. This event shaped the unique genetic landscape of the flowerpot snake. We examined gene expression specificity in ovarian tissues and identified pathways essential for DNA replication and repair. Our findings suggest a potential mechanism of homologous chromosome pairing during meiosis in allopolyploid parthenogenesis. This research provides insights into the evolutionary adaptations and genetic mechanisms underlying parthenogenesis in reptilian species, challenging traditional views on reproductive strategies and genomic evolution in asexual organisms. The genome of the flowerpot snake provides insights into triploid formation and parthenogenetic reproduction.