The adaptive genetic variation in response to heterogeneous habitats of the Indian Ocean was investigated in the Indian oil sardine using ddRAD sequencing to understand the subpopulation structure, stock complexity, mechanisms of resilience, and vulnerability in the face of climate change. Samples were collected from different ecoregions of the Indian ocean and ddRAD sequencing was carried out. Population genetic analyses revealed that samples from the Gulf of Oman significantly diverged from other Indian Ocean samples. SNP allele-environment correlation revealed the presence of candidate loci correlated with the environmental variables like annual sea surface temperature, chlorophyll-a, and dissolved oxygen concentration which might represent genomic regions allegedly diverging as a result of local adaptation. Larval dispersal modelling along the southwest coast of India indicated a high dispersal rate. The two major subpopulations (Gulf of Oman and Indian) need to be managed regionally to ensure the preservation of genetic diversity, which is crucial for climatic resilience.