IntroductionSustainable strategies are needed to remediate total petroleum hydrocarbon (TPH)-contaminated soils.MethodsA 90-day pot experiment combined soybean cultivation with different concentrations of nano-zinc oxide (nano-ZnO), followed by soil physicochemical, amplicon sequencing, microbial network, metabolomic, and multi-omics analyses.ResultsCombined application of soybean and 60 mg/kg nano-zinc oxide (nano-ZnO) significantly enhanced soil fertility and enzyme activities, achieving a 68.7% total petroleum hydrocarbon (TPH) removal rate over 90 days. Amplicon sequencing revealed soybean cultivation primarily structured bacterial and fungal communities. The rhizosphere buffered microbial diversity against TPH and nanoparticle stress, and co-occurrence networks showed the combined treatment fostered the most complex, stable cross-kingdom interactions. Soil metabolomics indicated a targeted rhizosphere response to nano-ZnO, enriching flavonoids and biosurfactant precursors, contrasting with the non-specific stress response in bare soil. Multi-omics integration identified a functional guild (Pseudomonas, Sphingomonas, Rhodococcus, and Fusarium) associated with TPH dissipation.DiscussionThese results suggest that soybean remodels its rhizosphere microbiome structure and metabolic function to synergize with nano-ZnO, accelerating the recovery of petroleum-contaminated soils.