Abstract Soil microorganisms found in the root zone impact plant growth and development, but the potential to harness these benefits is hampered by the sheer abundance and diversity of the players influencing desirable plant traits. Here, we report a high level of reproducibility of soil microbiomes in altering plant flowering time and soil functions when partnered within and between plant hosts. We used a multi-generation experimental system using Arabidopsis thaliana Col to select for soil microbiomes inducing earlier or later flowering times of their hosts. We then inoculated the selected microbiomes from the tenth generation of plantings into the soils of three additional A. thaliana genotypes (Ler, Be, RLD) and a related crucifer (Brassica rapa). With the exception of Ler, all other plant hosts showed a shift in flowering time corresponding with the inoculation of early- or late-flowering microbiomes. Analysis of the soil microbial community using 16 S rRNA gene sequencing showed distinct microbiota profiles assembling by flowering time treatment. Plant hosts grown with the late-flowering-associated microbiomes showed consequent increases in inflorescence biomass for three A. thaliana genotypes and an increase in total biomass for B. rapa. The increase in biomass was correlated with two- to five-fold enhancement of microbial extracellular enzyme activities associated with nitrogen mineralization in soils. The reproducibility of the flowering phenotype across plant hosts suggests that microbiomes can be selected to modify plant traits and coordinate changes in soil resource pools.