Egg-laying females of the seed beetle Callosobruchus maculatus discriminate against occupied (egg-laden) seeds, and thus reduce competition among larvae within seeds. Two strains (S and B) differed genetically in this trait. A factorial experiment was performed to distinguish whether greater avoidance of occupied hosts by S-strain females was caused by a stronger chemical deterrent associated with S-strain eggs, a keener response to the presence of eggs by S-strain females, or both. The degree of host discrimination depended on both the source of eggs and the source of test females; the strongest avoidance of egg-laden seeds was exhibited by S-strain females presented with clean seeds as opposed to seeds bearing S-strain eggs, whereas the weakest host discrimination was exhibited by B-strain females presented clean seeds as opposed to seeds bearing B-strain eggs. When presented with only egg-laden seeds, females from both strains added more eggs to seeds bearing B-strain eggs than to seeds bearing S-strain eggs, but the degree of discrimination between the two kinds of egg-laden seeds was stronger among S-strain females. Population differences in host discrimination appear to reflect differential costs associated with multiple larvae/seed; the more discriminating S strain has been associated with a relatively small host and its larvae engage in exceptionally strong interference competition.