Despite the effectiveness of microbial-phytoremediation for remediating total petroleum hydrocarbons (TPH)-contaminated soil, the underlying mechanisms remain elusive. This study investigated the whole-genome and biological activity of Rhodococcus erythropolis KB1, revealing its plant growth promotion (PGP), TPH degradation, and stress resistance capabilities. Phytoremediation (using alfalfa) and plant-microbial remediation (using alfalfa and KB1) were employed to degrade TPH. The highest TPH degradation rate, reaching 95%, was observed with plant-microbial remediation. This is attributed to KB1's ability to promote alfalfa growth, induce the release of signaling molecules to activate plant antioxidant enzymes, actively recruit TPH-degrading bacteria (e.g., Sphingomonas, Pseudomonas, C1-B045), and increase soil nitrogen and phosphorus levels, thereby accelerating TPH degradation by both plants and microorganisms. This study demonstrates that R. erythropolis KB1 holds great potential for enhancing the remediation of TPH-contaminated soil through its multifaceted mechanisms, particularly in plant-microbial remediation strategies, providing valuable theoretical support for the application of this technology.