Bacillus thuringiensis is one of the most useful bacteria in insect pest management: it is used as an environmentally friendly biopesticide and its insecticidal toxins are incorporated into genetically modified crops. Concerns for its ongoing economic exploitation include the rapidity with which insects can evolve resistance to its toxins and whether B. thuringiensis is ecologically and genetically distinct from closely related strains that cause infections in humans and domestic animals. We found that natural bacterial populations in soil and on cabbage leaves were dominated by an insect-pathogen specialist genotype, and this genotype was better than its close relatives at establishing populations on leaves where its hosts were likely to be feeding. Spraying microbial pesticides and the addition of insect hosts increased the proportion of insect-pathogen specialists in the bacterial population, confirming that application of these biopesticides is a safe means of insect control. Populations of B. thuringiensis were transient on plant material, suggesting that selective pressure for resistance can be similarly transient. However, the genotype that dominates the natural community has been economically exploited more than any other, and selection for resistance to this strain may have occurred in natural populations of insects prior to the use of B. thuringiensis in pest control.