The use of chemical fertilizers and pesticides has caused harmful impacts on the environment with the increase in economic burden. Biofertilizers are biological products containing living microorganisms capable of improving plant growth through eco-friendly mechanisms. In this work, three actinobacterial strains Streptomyces violaceoruber, Streptomyces coelicolor, and Kocuria rhizophila were characterized for multiple plant growth promoting (PGP) traits such as indole acetic acid production, phosphate solubilization, N₂-fixation, and drought and salt tolerance. Then, these strains were investigated for their secreted and cellular metabolome, revealing a rich arsenal of bioactive molecules, including antibiotics and siderophores, with S. violaceoruber being the most prolific strain. Furthermore, the in vivo assays, performed on tomato (Solanum lycopersicum L.), resulted in an improved germination index and the growth of seedlings from seeds treated with PGP actinobacteria, with a particular focus on S. violaceoruber cultures. In particular, this last strain, producing volatile organic compounds having antimicrobial activity, was able to modulate volatilome and exert control on the global DNA methylation of tomato seedlings. Thus, these results, confirming the efficacy of the selected actinobacteria strains in promoting plant growth and development by producing volatile and non-volatile bioactive molecules, can promote eco-friendly alternatives in sustainable agriculture.