Monitoring biodiversity in highly connected marine species is challenging because strong gene flow can obscure ecologically meaningful population differences. Conventional ecological and molecular surveys often interpret widely distributed marine organisms as genetically homogeneous, potentially overlooking cryptic variation relevant to resilience and conservation. Here, we show how whole-genome monitoring can uncover hidden genomic heterogeneity beneath apparent panmixia in the horn-eyed ghost crab Ocypode ceratophthalmus, a highly dispersive intertidal species distributed across the Indo-West Pacific. We generated the first high-quality reference genome (1.65 Gb) for O. ceratophthalmus and conducted whole-genome resequencing of 74 individuals sampled across 2,000 km of the southeastern coast of China. Genome-wide analyses consistently revealed extremely high connectivity and minimal spatial structure. Principal component analysis showed extensive clustering among populations, and ADMIXTURE supported shared ancestry, pairwise genetic differentiation was negligible, and no isolation-by-distance pattern was detected, collectively indicating near-panmixia across broad geographic scales. Despite this apparent genomic homogeneity, multi-scale analyses uncovered pronounced hidden heterogeneity in demographic history and population resilience. Demographic reconstruction showed that all populations experienced a shared Holocene bottleneck, suggesting a common response to historical coastal environmental change. However, the Guangdong population (GD) exhibited greater demographic persistence, with a weaker decline in effective population size, the fastest linkage disequilibrium decay, and asymmetric northward gene flow, indicating a likely role as a regional source population. Runs of homozygosity (ROH) analyses provided finer-scale evidence of hidden variation. Most ROH tracts were short (50–200 kb), consistent with historical rather than recent demographic processes. Notably, GD maintained significantly lower ROH burden and genomic inbreeding across length classes, indicating reduced homozygosity accumulation and stronger demographic resilience despite broad-scale panmixia. Recurrent ROH islands were also detected, suggesting that signatures of historical selection and local adaptation may persist under extensive genetic exchange. Our findings demonstrate that high connectivity does not necessarily imply demographic uniformity. By integrating whole-genome resequencing with demographic inference and ROH analyses, this study highlights the value of genomic monitoring for detecting cryptic heterogeneity in highly connected marine species and uncovering biologically meaningful variation masked by strong gene flow.