Background/Objectives: The swimming crab Charybdis feriata is an important commercial fishery species and a major economic contributor to the southeast coastal fishing communities in China. Under the scenario of resource decline and shortage in the market over recent years, it has become more urgent and necessary to explore the fine-scale population genetic characteristics of C. feriata. Methods: In this study, the genotyping-by-sequencing (GBS) method was used to estimate the genome-wide genetic variation in and population differentiation pattern of C. feriata collected from four geographical locations (Zhoushan, Quanzhou, Yangjiang, and Qinzhou) along the southeast coast of China. Results: A total of 18,815 high-quality single-nucleotide polymorphisms (SNPs) were identified and the results revealed the existence of high genetic diversity and low genetic divergence among the populations of C. feriata. Floating eggs and larvae transported by alongshore currents during the reproductive season might enhance the interpopulation genetic exchange. Principal component analysis (PCA) and a phylogenetic tree showed a high genetic connectivity of C. feriata across the southeast coast of China, but C. feriata distributed in the Zhoushan Archipelago might possess some genetic distinctiveness and diversification. Conclusions: The results supplemented basic genetic information of C. feriata at the genome level and also provided specific knowledge that could lead to the improved spatial management of fishery resources.