Variation in life histories among populations of cactophilicDrosophila mojavensis has been hypothesized to be a by-product of a shift to one of two alternate host plants. When cultured on the ancestral and a secondary host cactus, a Baja population expressed shorter development times and smaller thorax sizes than a mainland population, but viability did not differ. Comparisons with all reciprocal F1 and F2 crosses between populations revealed that genetic differences in development time and thorax size were largely additive. Homeostasis in these life history traits was population specific, except for viability. Homeostasis in development time was greater in the Baja population than in the other crosses, suggesting dominance for decreased homeostasis in the mainland population. Underdominance in viability homeostasis of the F1 hybrids suggested some incompatibility between populations. Homeostasis in thorax size was greater in females than in males and differed among parental populations. Maintenance of heritable differences and genetic variation for homeostasis in these traits suggested a role for cactus-specific differences in environmental uncertainty caused by variation in breeding site duration and abundance in nature.