Pseudomonas protegens shows a high degree of lifestyle plasticity since it can establish both plant-beneficial and insect-pathogenic interactions. While P. protegens protects plants against soilborne pathogens, it can also invade insects when orally ingested leading to the death of susceptible pest insects. The mechanism whereby pseudomonads effectively switch between lifestyles, plant-beneficial or insecticidal, and the specific factors enabling plant or insect colonization are poorly understood. We generated a large-scale transcriptomics dataset of the model P. protegens strain CHA0 which includes data from the colonization of wheat roots, the gut of Plutella xylostella after oral uptake and the Galleria mellonella hemolymph after injection. We identified extensive plasticity in transcriptomic profiles depending on the environment and specific factors associated to different hosts or different stages of insect infection. Specifically, motor-activity and Reb toxin-related genes were highly expressed on wheat roots but showed low expression within insects, while certain antimicrobial compounds (pyoluteorin), exoenzymes (a chitinase and a polyphosphate kinase), and a transposase exhibited insect-specific expression. We further identified two-partner secretion systems as novel factors contributing to pest insect invasion. Finally, we use genus-wide comparative genomics to retrace the evolutionary origins of cross-kingdom colonization.