The diversity of insect eggs is astounding but still largely unexplained. Here, we apply phylogenetic analyses to 208 species of stick and leaf insects, coupled with physiological measurements of metabolic rate and water loss on five species, to evaluate classes of factors that may drive egg morphological diversification: life history constraints, material costs, mechanical constraints, and ecological circumstances. We show support for all three classes, but egg size is primarily influenced by female body size and strongly trades off with egg number. Females that lay relatively fewer but larger eggs, which develop more slowly because of disproportionately low metabolic rates, also tend to bury or glue them in specific locations instead of simply dropping them from the foliage (ancestral state). This form of parental care then directly favors relatively elongated eggs, which may facilitate their placement and allow easier passage through the oviducts in slender species. In addition, flightless females display a higher reproductive output and consequently lay relatively more and larger eggs compared with flight-capable females. Surprisingly, local climatic conditions had only weak effects on egg traits. Overall, our results suggest that morphological diversification of stick insect eggs is driven by a complex web of causal relationships among traits, with dominant effects of resource allocation and oviposition strategies, and of mechanical constraints.