The impact of oil pollution on coastal vulnerable ecosystems has been a major concern especially, in the Persian Gulf area. The current study was carried out to assess to what extent Avicennia marina can tolerate oil contamination and degrade crude oil polycyclic aromatic hydrocarbons (PAHs) from rhizosphere soil. Seeds of A. marina were grown in control and crude oil-contaminated (2.5, 5.0, 7.5, and 10% w/w) soil under ambient greenhouse conditions. Four-month-old plants were collected, measured for their biometry, and assayed for physiological characteristics in relation to degradation of PAHs. A. marina exposed to petroleum responded by allocating proportionally more biomass to root than shoot, activating enzymatic and non-enzymatic antioxidative mechanisms and removing of PAHs, particularly in lower concentrations of crude oil in the soil. The content of total PAHs in A. marina rhizosphere soil, grown on 2.5, 5.0, 7.5 and 10% oil-treated soils were, respectively, 37 ± 0.4, 21.84 ± 0.27, 12.78 ± 0.11 and 14.74 ± 0.03% lower than non-rhizosphere soil. Comparison of PAHs content of rhizospheric and non-rhizospheric soil also indicated that the highest rate of PAH removal was for acenaphthene (74.63 ± 0.78) in control, fluoranthene (71.18 ± 0.56) in 2.5%, and anthracene (69.45 ± 6.33, 55.66 ± 4.38 and 35.97 ± 0.22) in 5.0, 7.5 and 10% oil-contaminated soil and acenaphthene (74.63 ± 0.78) in control. Activities of peroxidase, ascorbate peroxidase, and polyphenol oxidase were more prominent in the roots of plants exposed to increasing concentrations of oil in soil than control plants. Conversely, the activity of superoxide dismutase decreased. These findings render A. marina as a phytoremediation candidate for small scale oil spills and residual oil pollution in coastal marine environments.