Cholera caused by Vibrio cholerae serogroup O139 was first reported in Bangladesh and India in 1992 and subsequently and rapidly spread to other parts of Asia. To understand the genomic epidemiology and origins of V. cholerae O139 in China, we sequenced the genomes of 104 V. cholerae O139 isolates from 1994 to 2018 in Zhejiang, a southeast coastal province in China and compared with 57 publicly available V. cholerae O139 genomes from other Asian countries. Phylogenomic analysis found that there were two major lineages and Zhejiang isolates were further clustered as 3 clusters and a few outliers. Cluster 1 within lineage 1 and clusters 2 and 3 withing lineage 2 were likely to have originated from India and Thailand respectively during early 1990s. The three clusters were successively replaced between 1994 and 2018. Cluster 1 was found in 1996 and persisted until 2000, Cluster 2 from 1998 to 2008 and Cluster 3 from 1998 to 2018. Carriage of antibiotic resistance genes by Chinese isolates exhibited many cluster-specific antimicrobial resistance (AMR) genes, including blaTEM-1, catA2, aac(3)-lld, aadA2, aph(3’)-la, mph(E), msr(E), sul, dfrA12, tet(M) and tet(Y). Additionally, quinolone resistance conferring mutations S85L and S83I occurred in 71.2% of Chinese isolates. We also found that the copy number of ctxB gene varied from 2 to 22 and differed among the three clusters with cluster 2 carrying an average of 4.4 copies. This study has shed light on the spread of V. cholerae O139 into China.