Plants of different genotypes and physiological states recruit different populations of root microbiota. The selection is driven by the immune response of the plant and the composition of root exudates. Some bacteria, including Pseudomonas spp., are promiscuous root colonizers. It is yet unclear what particular changes in lifestyle enable them to thrive in the company of different plant hosts. In this study, we used RNAseq to identify genes of the differential (host-specific) and shared (host-independent) transcriptomic responses of a biocontrol strain Pseudomonas donghuensis P482 to the root exudates of two phylogenetically distinct plant species, tomato (Dicot) and maize (Monocot), both of which can be colonized by the bacterium. The host-independent response of P482 to exudates involved upregulated expression of arsenic resistance genes and bacterioferritin synthesis. Contrary, we observed downregulation of pathways related to sulfur assimilation, sensing of ferric citrate and/or other iron carriers, the acquisition of heme, the assembly of the type VI secretion system, and amino acid transport. Pathways upregulated in P482 specifically by tomato exudates included nitric oxide detoxification, repair of iron-sulfur clusters, respiration through the cyanide-insensitive cytochrome bd, and catabolism of amino acids and/or fatty acids. The maize-specific response included upregulation of genes associated with motility, the activity of MexE and two other RND efflux pumps, and copper tolerance. To provide more context to the study, we determined the chemical composition of exudates by GC-MS, NMR, and LC-SRM. Our results bring new insight into the host-driven metabolic adaptations of promiscuous root colonizing bacteria.