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This study investigated the polycyclic aromatic hydrocarbons (PAHs) occurrence, and their impact on the microbial community and PAH-degrading genera and genes in the Knysna Estuary of South Africa. The results reveal that the estuary exhibits low PAH levels (114.1–356.0 ng g−1). Ignavibacteriae and Deferribacteres, as well as Proteobacteria and Bacteroidetes, are keystone phyla. Among measured environmental factors, total organic carbon (TOC), nutrients such as nitrite and nitrate, metals as Al, Cr, Cu, Ni, Pb and Zn, and environmental properties (pH and salinity) are primary contributors to structuring the bacterial community assemblage. The abundance of alpha subunit genes of the PAH-ring hydroxylating dioxygenases (PAH-RHDα) of Gram-negative bacteria lies in the range of (2.0–4.2) × 105 copies g−1, while that of Gram-positive bacteria ranges from 3.0 × 105 to 1.3 × 107 copies g−1. The PAH-degrading bacteria account for up to 0.1% of the bacterial community and respond mainly to nitrate, TOC and salinity, while PAHs at low concentration are not significant influencing factors. PAH degraders such as Xanthomonadales, Pseudomonas, and Mycobacterium, which play a central role in PAH-metabolization coupled with other biogeochemical processes (e.g. iron cycling), may contribute to maintaining a healthy estuarine ecosystem. These results are important for developing appropriate utilization and protection strategies for pristine estuaries worldwide.