The objectives of this study were (1) to determine the impact of severe zinc deficiency on the establishment, growth, survival and reproduction of Heligmosomoides polygyrus in the laboratory mouse, during both primary and challenge infection protocols, and (2) to determine whether the observed effects resulted from zinc deficiency per se, or from the accompanying energy restriction. Three diet groups were used: zinc-sufficient (Zn+: 60 mg zinc/kg diet), zinc-deficient (Zn·75 mg zinc/kg diet) and energy restricted (ER: 60 mg zinc/kg diet pair fed to Zn− mice). Neither Zn− nor ER influenced the establishment of the parasite during a primary infection. However, both significantly influenced the early development of the parasite. The proportion of adult worms recovered 9 days post-infection (p.i.) was highest in Zn− mice, intermediate in ER mice and lowest in +Zn+ mice. Worms were also distributed more distally in the intestine of the Zn− mice and worm survival was highest in Zn− mice, intermediate in ER mice and lowest in Zn+ mice at both 4 and 5 weeks p.i. Although the length of female worms was reduced in Zn− mice, neither per capita fecundity nor egg viability was affected by zinc deficiency. Energy restriction, on the other hand, significantly reduced worm fecundity at 5 weeks post-primary infection, but had no effect on egg viability. Zinc concentration of adult H. polygyrus was similar among dietary groups. The effects of zinc deficiency and energy restriction were also investigated 4 and 5 weeks after a challenge infection. Whereas strong host resistance was evident in Zn+ and ER mice, based on comparison of worm numbers between challenged mice and primary infection controls, no evidence of resistance was detected in Zn− mice. As in the primary infection, female worms were shorter in Zn− mice than in ER and Zn+ mice, and energy restriction but not zinc deficiency significantly affected per capita fecundity. However, in contrast to the primary infection, ER mice had elevated rather than reduced fecundity. This study demonstrates a complex interaction between H. polygyrus and zinc and energy restriction, and highlights the importance of controlling for reduced food intake in nutrition–infection studies.