Natural populations vary tremendously in their susceptibility to infectious disease agents. The factors (environmental or genetic) that underlie this variation determine the impact of disease on host population dynamics and evolution, and affect our capacity to contain disease outbreaks and to enhance resistance in agricultural animals and disease vectors. Here, we show that changes in the environmental conditions under which female Daphnia magna are kept can more than halve the susceptibility of their offspring to bacterial infection. Counter-intuitively, and unlike the effects typically observed in vertebrates for transfer of immunity, mothers producing offspring under poor conditions produced more resistant offspring than did mothers producing offspring in favourable conditions. This effect occurred when mothers who were well provisioned during their own development then found themselves reproducing in poor conditions. These effects likely reflect adaptive optimal resource allocation where better quality offspring are produced in poor environments to enhance survival. Maternal exposure to parasites also reduced offspring susceptibility, depending on host genotype and offspring food levels. These maternal responses to environmental conditions mean that studies focused on a single generation, and those in which environmental variation is experimentally minimized, may fail to describe the crucial parameters that influence the spread of disease. The large maternal effects we report here will, if they are widespread in nature, affect disease dynamics, the level of genetic polymorphism in populations, and likely weaken the evolutionary response to parasite-mediated selection.