Endophytes with plant growth-promoting activity can improve the health and development of plants during all life stages. However, less is known about their stability and transmission across plant genotypes, habitats, and generations. By combining community and isolate analyses, we found that each plant habitat and genotype harbored distinct bacterial communities and plant growth-promoting bacteria (PGPB). Soil, root endosphere, and rhizosphere were the habitats with the highest bacterial diversity, while seeds hosted more selective communities. Seeds generated under field conditions showed traces of a bacterial community composition connected to the suppression of plant pathogens. In contrast, seeds of the successive generation grown in a pathogen-free and low-nutrient environment showed a predominance of bacteria that facilitate the uptake of nutrients. These modifications of the microbiome can be explained by an adaptation to prevalent environmental conditions. Cultivation approaches revealed microhabitat-specific PGPB that were assigned to various species of Bacillus, Stenotrophomonas, and Ralstonia. Tracking down these bacteria among the whole tomato plant allowed us to identify the seed as a primary vehicle of PGPB transmission. This previously undescribed vertical transmission of PGPB represents a strategy to maintain plant beneficial bacteria over generations and has an impact for the design of seed treatments.