Schistosoma japonicum, prevalent in East and Southeast Asia, is a zoonotic parasite that causes human schistosomiasis. The evolutionary history and local adaptation of S. japonicum are poorly known due to the lack of high-quality whole-genome data. We assembled a chromosome-level genome of S. japonicum and analyzed the genomes of 72 S. japonicum collected from six populations covering its entire endemic region. We studied a zoophilic lineage from Taiwan that was primarily separated from other zoonotic populations at ~45 Kya. This is consistent with the divergent history of their intermediate hosts. A severe population bottleneck was detected in S. japonicum during the Last Glacial Maximum, that coincided with demographic history of the modern humans in Asia. We identified several genomic regions likely underlying positive selection. For example, GATAD2A showed substantial differentiation between the zoophilic and zoonotic populations. RNAi knockdown suggested that it is associated with parasite development and infection establishment in definitive hosts. Another example was Lmln, a protein-coding gene associated with the specificity of the intermediate hosts, that showed divergent adaptation between mountain and lake areas. These findings provide a comprehensive set of population-genomic data and a genomic resource for further functional and medical studies.