Plants host a large array of commensal bacteria that interact with the host. The growth of both bacteria and plants is often dependent on nutrients derived from the cognate partners, and the bacteria fine-tune host immunity against pathogens. This ancient interaction is common in all studied land plants and is critical for proper plant health and development. We hypothesized that the spatial vicinity and the long-term relationships between plants and their microbiota may promote or even depend on cross-kingdom horizontal gene transfer (HGT), a phenomenon that is relatively rare in nature. To test this hypothesis we analyzed the Arabidopsis thaliana genome and its extensively sequenced microbiome to detect events of horizontal transfer of full length genes that are absent from non-plant associated bacteria. Interestingly, we detected 180 unique genes that were horizontally transferred between plants and their microbiota. Genes transferred from plants to their microbiota are enriched in secreted proteins that metabolize carbohydrates, whereas microbes transferred to plants genes that are enriched in redox homeostasis functions. To validate our approach, we tested if a bacterial gene is functionally similar to its Arabidopsis homologue in planta. The Arabidopsis DET2 gene is essential for biosynthesis of the brassinosteroid phytohormones and loss-of-function of the gene leads to dwarfism. We found that expression of the DET2 homologue from Leifsonia bacteria of the Actinobacteria phylum in the Arabidopsis det2 background complements the mutant, and leads to normal plant growth. Together, these data suggest that cross-kingdom horizontal gene transfer events shape the interactions between plants and their microbiome.