Inconsistencies in the relationship between fluctuating asymmetry (FA) and fitness may be due to selection acting on the degree of trait asymmetry that differs among populations or among traits. We assessed relationships between parasite susceptibility and fluctuating asymmetry in the number of bony lateral plates among 83 populations of freshwater Gasterosteus aculeatus (three spined stickleback) and among lateral plate positions that vary in the selection they experience for symmetry. The correlation between FA and parasite infection was highly variable among samples. Excess of infected asymmetric G. aculeatus increased significantly as the robustness of structural predator defences decreased. This effect was found for one parasite species only (Eustrongylides sp.) and was slightly stronger in females. In addition, there was a trend for there to be an excess of infected females asymmetric in those lateral plates positions that did not experience selection for their symmetry, although the trend only approached significance. These results suggest that selection for trait symmetry can obscure relationships between fitness and individual-wide developmental stability, providing one possible explanation for some of the heterogeneity in FA/fitness relationships seen in the literature. These results are also consistent with previous reports showing that ecological segregation between symmetric and asymmetric G. aculeatus and between sexes can alter the FA/fitness relationship.