The Persian Gulf, hosting ca. 48% of the world's oil reserves, has been chronically exposed to natural oil seepage. Oil spill studies show a shift in microbial community composition in response to oil pollution; however, the influence of chronic oil exposure on the microbial community remains unknown. We performed genome-resolved comparative analyses of the water and sediment samples along Persian Gulf's pollution continuum (Strait of Hormuz, Asalouyeh, and Khark Island). Continuous exposure to trace amounts of pollution primed the intrinsic and rare marine oil-degrading microbes such as Oceanospirillales, Flavobacteriales, Alteromonadales, and Rhodobacterales to bloom in response to oil pollution in Asalouyeh and Khark samples. Comparative analysis of the Persian Gulf samples with 106 oil-polluted marine samples reveals that the hydrocarbon type, exposure time, and sediment depth are the main determinants of microbial response to pollution. High aliphatic content of the pollution enriched for Oceanospirillales, Alteromonadales, and Pseudomonadales whereas, Alteromonadales, Cellvibrionales, Flavobacteriales, and Rhodobacterales dominate polyaromatic polluted samples. In chronic exposure and oil spill events, the community composition converges towards higher dominance of oil-degrading constituents while promoting the division of labor for successful bioremediation.