The Indo-Pacific humpback dolphin (Sousa chinensis; hereafter IPH dolphin), a coastal cetacean species primarily distributed in Chinese waters, serves as a flagship species for marine ecosystem conservation. Currently, this species faces sustained population declines and habitat degradation, and is listed as "Vulnerable" on the IUCN Red List. Herein, we de novo assembled a high-quality chromosome-level genome for the IPH dolphin and conducted conservation genomic analyses using whole-genome resequencing data from 82 individuals across four major geographic populations in Chinese waters (northern Beibu Gulf (NBG), eastern Zhanjiang (EZJ), Pearl River Estuary (PRE), and Xiamen (XM)) and one population from the Gulf of Thailand (THA). Our findings reveal that the four Chinese populations form three genetic clusters, with PRE and XM merging into one. Historical fluctuations in the effective population size (Ne) of IPH dolphins correlate with sea-level changes, while recent declines and critically low Ne now characterize all four Chinese populations. Gene flow was detected between NBG and EZJ, and between EZJ and PRE, indicating high historical population connectivity. Alarmingly, all four Chinese populations exhibited extremely low genetic diversity and elevated inbreeding levels. Genes carrying loss-of-function mutations in IPH dolphins were enriched in pathways related to DNA repair and cellular responses to organonitrogen compounds, potentially increasing cancer susceptibility and impairing the responses to aquatic organic pollutants. In conclusion, given the extremely low Ne and limited genetic evolutionary potential of IPH dolphins in Chinese waters, coupled with unfavorable marine environmental conditions, urgent conservation measures are warranted.