Portunus trituberculatus (Crustacea: Decapoda: Brachyura), commonly known as the swimming crab, is of major ecological importance, as well as being important to the fisheries industry. P. trituberculatus is also an important farmed species in China due to its rapid growth rate and high economic value. Here, we report the genome sequence of the swimming crab, which was assembled at the chromosome scale, covering ~1.2 Gb, with 79.99% of the scaffold sequences assembled into 53 chromosomes. The contig and scaffold N50 values were 108.7 kb and 15.6 Mb, respectively, with 19,981 protein-coding genes and a high proportion of simple sequence repeats (49.43%). Based on comparative genomic analyses of crabs and shrimps, the C2H2 zinc finger protein family was found to be the only gene family expanded in crab genomes, and its members were mainly expressed in early embryonic development and during the flea-like larval stage, suggested it was closely related to the evolution of crabs. Combined with transcriptome and Bulked Segregant Analysis (BSA) providing insights into the genetic basis of salinity adaptation in P. trituberculatus, strong immunity and rapid growth of the species were also observed. In addition, the specific region of the Y chromosome was located for the first time in the genome of P. trituberculatus, and Dmrt1 was identified as a key sex determination gene in this region. Decoding the swimming crab genome not only provides a valuable genomic resource for further biological and evolutionary studies, but is also useful for molecular breeding of swimming crabs.