Endophytic fungi offer promising alternatives for sustainable plant disease management strategies, often through the production of bioactive secondary metabolites. This study investigated the biocontrol potential of filtrates and extracts, produced under controlled conditions, from Alternaria leptinellae E138 against Pseudomonas syringae in tomato plants under greenhouse conditions. To understand the main mechanisms involved in biocontrol, the direct inhibition of bacterial growth and disruption of quorum sensing activity caused by metabolites were studied in vitro, as well as indirect mechanisms, such as their capacity to produce phytohormone-like substances, nutrient mobilization, and antioxidant activity, which can enhance plant growth and fitness. Moreover, a mass spectrometry analysis was used to tentatively identify the secondary metabolites present in the extract with antimicrobial properties, which could explain the biocontrol effects observed. Mycopriming assays, involving the direct treatment of tomato seeds with the fungal A. leptinellae E138 extracts, produced increased germination rates and seedling vigor in tomato seeds. As another treatment, postemergence application of the extracts in greenhouse conditions significantly improved plant health and resulted in a 41% decrease in disease severity. Overall, this study underscores the potential of A. leptinellae E138 extract as a plant growth promoter with biocontrol capabilities, offering promising avenues for sustainable plant disease management.