The level of habitat availability influences genetic divergence among populations and the genetic diversity within populations. In the marine environment, near-shore species are among the most sensitive to habitat changes. Knowledge of how historical environmental change affected habitat availability and genetic variation can be applied to the development of proactive management strategies of exploited species. Here, we modeled the contemporary and historical distribution of Lutjanus jocu in Brazil. We describe patterns of genomic diversity to better understand how climatic cycles might correlate with the species demographic history and current genetic structure. We show that during the Last Glacial Maximum, there were ecological barriers that are absent today, possibly dividing the range of the species into three geographically separated areas of suitable habitat. Consistent with a historical reduction in habitat area, our analysis of demographic changes shows that L. jocu experienced a severe bottleneck followed by a population size expansion. We also found an absence of genetic structure and similar levels of genetic diversity throughout the sampled range of the species. Collectively, our results suggest that habitat availability changes have not obviously influenced contemporary levels of genetic divergence between populations. However, our demographic analyses suggest that the high sensitivity of this species to environmental change should be taken into consideration for management strategies. Furthermore, the general low levels of genetic structure and inference of high gene flow suggest that L. jocu likely constitutes a single stock in Brazilian waters and, therefore, requires coordinated legislation and management across its distribution.