In seasonal populations, vital rates are not only determined by the direct effects of density at the beginning of each season, but also by density at the beginning of past seasons. Such delayed density dependence can arise via non-lethal effects on individuals that carry over to influence per capita rates. In this study, we examine (i) whether parental breeding density influences offspring size, (ii) how this could carry over to affect offspring survival during the subsequent non-breeding period and (iii) the population consequences of this relationship. Using Drosophila melanogaster, the common fruit fly, submitted to distinct breeding and non-breeding seasons, we first used a controlled laboratory experiment to show that high parental breeding density leads to small offspring size, which then affects offspring survival during the non-breeding period but only at high non-breeding densities. We then show that a model with the interaction between parental breeding density and offspring density at the beginning of the non-breeding season best explained offspring survival over 36 replicated generations. Finally, we developed a biseasonal model to show that the positive relationship between parental density and offspring survival can dampen fluctuations in population size between breeding and non-breeding seasons. These results highlight how variation in parental density can lead to differences in offspring quality which result in important non-lethal effects that carry over to influence per capita rates the following season, and demonstrate how this phenomenon can have important implications for the long-term dynamics of seasonal populations.