<p>Geological history, including tectonic activity and sea-level changes, dispersal capability, and habitat continuity, are among the key players in shaping the phylogeography of marine species. The Persian Gulf is a shallow semi-enclosed marginal sea in the northwestern part of the Indian Ocean with harsh physical conditions. A variety of population structures have been revealed for different taxa of this area. In this study, we aim to address the population structure and demography of the native intertidal mudflat crab, <i>Nasima dotilliformis</i>, along the Persian Gulf, the Strait of Hormuz, and the Gulf of Oman, using morphological and genetic analyses. Nineteen morphometric characters, carapace shape variations, and mitochondrial marker (COI) were analyzed. Morphometric and geometric-morphometric analyses revealed population differentiations among the three regions, with the Persian Gulf being more distinctive. Genetic comparisons also confirmed the partial isolation of the Persian Gulf from the other two regions. As this species is an obligate inhabitant of intertidal muddy substrates, we hypothesize that habitat discontinuity between stations in the Persian Gulf and the Strait of Hormuz may be the primary driver of this differentiation. Demographic analyses (mismatch distribution and neutrality tests) show evidence of strong genetic drift in this species along the study area. We hypothesize that this species may be experiencing a bottleneck effect as a result of population collapse during the Last Glacial Maximum (LGM) when their muddy substrate was scarce. We believe that our results provide new insights to be considered in conservation actions to protect such a native species which has been morphologically/genetically isolated in the Persian Gulf.</p>