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Abstract Parthenogenetic wasps provide an ideal natural experiment to study the heritability, plasticity, and microevolutionary dynamics of body size. Dinocampus coccinellae (Hymenoptera:Braconidae, Euphorinae) is a solitary, generalist braconid parasitoid wasp that reproduces through thelytokous parthenogenesis, and parasitizes over fifty diverse species of coccinellid ladybeetles worldwide as hosts. Here we designed an experiment with parthenogenetic lines of D. coccinellae presented with three different host ladybeetle species of varying sizes, across multiple generations to investigate heritability, and plasticity of body size measured via a combination of morphometric variables such as thorax width, abdominal width, and wing length in D. coccinellae. 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. Our results indicate (1) little heritable variation in body size, (2) strong independence of offspring size on the host environment, (3) small mothers produce larger offspring, and vice versa, independent of host. We then model the evolution of size and host-shifting under a constrained fecundity advantage model of Cope’s Law using a Hidden Markov Model, showing that D. coccinellae likely has fitness advantages to maintain plasticity in body size despite parthenogenetic reproduction.