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<i>Metarhizium brunneum</i> is a soil-borne fungal entomopathogen that can be associated with plant roots. Previous studies have demonstrated that root colonization by beneficial fungi can directly affect soil-borne pathogens through competition and antibiosis and can activate a systemic response in plants, resulting in a primed state for a faster and/or stronger response to stressors. However, the mechanisms by which <i>Metarhizium</i> inoculation ameliorates symptoms caused by plant pathogens are not well known. This study evaluated the ability of <i>M. brunneum</i> to protect oilseed rape (<i>Brassica napus</i> L.) plants against the soil-borne pathogen <i>Verticillium longisporum</i> and investigated whether the observed effects are a result of direct interaction and/or plant-mediated effects. In vitro and greenhouse experiments were conducted to measure fungal colonization of the rhizosphere and plant tissues, and targeted gene expression analysis was used to evaluate the plant response. The results show that <i>M. brunneum</i> delayed pathogen colonization of plant root tissues, resulting in decreased disease symptoms. Direct competition and antibiosis were found to be part of the mechanisms, as <i>M. brunneum</i> growth was stimulated by the pathogen and inhibited the in vitro growth of <i>V. longisporum</i>. Additionally, <i>M. brunneum</i> changed the plant response to the pathogen by locally activating key defense hormones in the salicylic acid (SA) and abscisic acid (ABA) pathways. Using a split-root setup, it was demonstrated that there is a plant-mediated effect, as improved plant growth and decreased disease symptoms were observed when <i>M. brunneum</i> was in the systemic compartment. Moreover, a stronger systemic induction of the gene <i>PR1</i> suggested a priming effect, involving the SA pathway. Overall, this study sheds light on the mechanisms underlying the protective effects of <i>M. brunneum</i> against soil-borne pathogens in oilseed rape plants, highlighting the potential of this fungal entomopathogen as a biocontrol agent in sustainable agriculture.