This study investigates the effects of metabolites from the beneficial bacteria Pseudomonas N5.12 formulated as silver nanoparticles (AgNPs) on tomato plants and soil microbial communities, to explore environmental safety of AgNPs for future applications in agriculture. AgNPs coated with bacterial metabolites are endowed with biological activity that is dose dependent, as shown by cytoskeleton alterations in Arabidopsis roots. The results show that N5.12-AgNPs can trigger beneficial effects on tomato plants, either when delivered through the leaves or roots, indicating effectiveness of the metabolites formulated as NP. Effects consist of lowering oxidative stress metabolism and therefore, improving plant resilience, as well as increasing chlorophyll a and carotenoid content. The significant reduction of H2O2 content was not associated to ROS scavenging enzymes but to an increase in total phenolic content. On the other hand, AgNPs had a minimal impact on bacterial metabolic activity, irrespective of the application way. Microbial communities’ structure was not altered by AgNP, anticipating environmental safety for agronomic applications. These findings suggest that Pseudomonas N5.12 metabolites formulated in AgNPs, at physiological concentration (30 ppm), may offer agricultural benefits by improving plant health appearing as an environmentally safe alternative for agriculture.