Marginal seas, surrounded by continents with dense populations, are vulnerable and have a quick response to climate change effects. The seas typically have alternatively rotating layered circulations to regulate regional heat and biogeochemical transports. The circulations are composed of dynamically active hotspots and governed by the couplings between unique extrinsic inflow and intrinsic dynamic response. Ambiguities about the circulations’ structure, composition, and physics still exist, and these ambiguities have led to poor numerical simulation of the marginal sea in global models. The South China Sea is an outstanding example of a marginal sea that has this typical rotating circulation. Our study demonstrates that the rotating circulation is structured by energetic hotspots with large vorticity arising from unique dynamics in the marginal sea and is identifiable by the constraints of Stokes Theorem. These hotspots contribute most of the vorticity and most of energy needed to form and maintain the rotating circulation pattern. Our findings provide new insights on the distinguishing features of the rotating circulation and the dominant physics with the objectives of advancing our knowledge and improving modeling of marginal seas.