The interaction of plants with the complex microbial networks that inhabit them is important for plant health. While the reliance of plants on their microbial inhabitants for defense against invading pathogens is well documented, the acquisition of data concerning the relationships between plant developmental stage or aging, and microbiome assembly, is still underway. In this work, we observed developmental-age dependent changes in the phyllopshere microbiome of tomato. The plant hormone cytokinin (CK) regulates various plant growth and developmental processes. Here, we show that age-related shifts in microbiome content vary based on content of, or sensitivity to, CK. We observed a developmental age associated decline in microbial richness and diversity, accompanied by a decline in the presence of growth promoting and resistance inducing bacilli in the phyllosphere. This decline was absent from CK-rich or CK-hypersensitive genotypes. Bacillus isolates we obtained from CK rich genotypes were found to re-program the transcriptome to support morphogenesis and alter the leaf developmental program when applied to seedlings, and enhance yield and agricultural productivity when applied to mature plants. Our results support the notion that CK-dependent effects on microbiome content support developmental functions, suggesting that these are mediated by CK in part via the bacterial community.