Abstract Dinocampus coccinellae (Hymenoptera:Braconidae, Euphorinae) is a solitary, generalist Braconid parasitoid wasp that reproduces through thelytokous parthenogenesis, an asexual process in which diploid daughters emerge from unfertilized eggs, and uses over fifty diverse species of coccinellid ladybeetles worldwide as hosts. Here we utilized a common garden and reciprocal transplant experiment using parthenogenetic lines of D. coccinellae presented with three different host ladybeetle species of varying sizes, across multiple generations to investigate heritability, plasticity, and environmental covariation of body size. We expected positively correlated parent-offspring parasitoid regressions, indicative of heritable size variation, from unilineal (parent and offspring reared on same host species) lines, since these restrict environmental variation in phenotypes. In contrast, because multilineal (parent and offspring reared on different host species) lines would induce phenotypic plasticity of clones reared in varying environments, we expected negatively correlated parent-offspring parasitoid regressions. Contrary to expectations, our results indicate (1) little heritable variation in body size, (2) strong independence of offspring size on the host environment, (3) a consistent signal of size-host tradeoff wherein small mothers produced larger offspring, and vice versa, independent of host environment. Our study offers support for a constrained fecundity advantage model of Cope’s Law, wherein D. coccinellae maintains phenotypic plasticity in body size despite parthenogenetic reproduction.