Microbial communities play a crucial role in supporting plant health and productivity. Reproducible, natural plant-associated microbiomes can help disentangle microbial dynamics across time and space. Here, using a sequential propagation strategy, we generated a complex and reproducible wheat rhizosphere microbiome (RhizCom) to study successional dynamics and interactions between the soil and heritable seed-borne rhizosphere microbiomes (SbRB) in a microcosm. Using 16S rRNA sequencing and genome-resolved shotgun metagenomics, we find that SbRB surpassed native soil microbes as the dominant rhizosphere-associated microbiome source. SbRB genomes were enriched in host-associated traits including degradation of key saccharide (niche partitioning) and cross-feeding interactions that supported partner strains (niche facilitation). In vitro co-culture experiments confirmed that helper SbRB strains facilitated the growth of partner bacteria on disaccharides as sole carbon source. These results reveal the importance of seed microbiota dynamics in microbial succession and community assembly, which could inform strategies for crop microbiome manipulation.