Fungal phytopathogens are challenging to control due to their penetration into plant tissues. Therefore, plant-colonizing bacteria could serve as an excellent weapon in fighting fungal infections. In this study, we aim to determine the biocontrol potential of the new endophytic strain Serratia quinivorans KP32, isolated from the roots of Petroselinum crispum L.; identify the related mechanisms; and understand the basis of its antagonistic interaction with taxonomically diverse fungi at the molecular level. The KP32 strain presented biological activity against Rhizoctonia solani, Colletotrichum dematium, Fusarium avenaceum, and Sclerotinia sclerotiorum, and its ability to inhibit the growth of the phytopathogens was found to be mediated by a broad spectrum of biocontrol features, such as the production of a number of lytic enzymes (amylases, chitinases, and proteases), siderophores, volatile organic and inorganic compounds, salicylic acid, and N-acyl-homoserine lactones. The higher expression of chitinase (chiA) and genes involved in the biosynthesis of hydrogen cyanide (hcnC), enterobactin (entB), and acetoin (budA) in bacteria exposed to fungal filtrates confirmed that these factors could act in combination, leading to a synergistic inhibitory effect of the strain against phytopathogens. We also confirm the active movement, self-aggregation, exopolysaccharide production, and biofilm formation abilities of the KP32 strain, which are essential for effective plant colonization. Its biological activity and colonization potential indicate that KP32 holds tremendous potential for use as an active biopesticide and plant growth promoter.