Within the marine environment, per offspring investment (POI) is associated with modes in larval development; an increase in POI has often been described with a decrease in temperature, as evidenced along latitudinal clines. However, the environmental drivers of POI remain largely hypothetical and have not yet been tested within an evolutionary context. Here, we test the hypothesis that developmental temperature is linked to POI within a globally distributed and diverse family of benthic crustaceans, the Lithodidae, also known as stone or king crab. To do this, we examine variations in egg diameter—a proven corollary of POI—within the Lithodidae. Based on a rare case of well-construed phylogeny, we test the relationship between egg diameter and two aspects of the maternal physical environment: water depth and temperature. We observe a significant relationship between decreasing environmental temperature and an increase in POI within genera of lithodid crabs, and independent of depth. There is a clear correlation of high levels in POI with a decrease in temperature in lithodid crab genera currently inhabiting the deep sea, all of which follow a food-independent (lecithotrophic) mode of larval development. In contrast, lithodid genera thriving in the warmer waters of shallow (continental shelf) seas follow a feeding (planktotrophic) mode in larval development. We conclude that temperature is an important factor governing POI, and discuss its importance in the evolution of larval lecithotrophy in marine invertebrates.Electronic supplementary materialThe online version of this article (doi:10.1007/s00227-015-2776-8) contains supplementary material, which is available to authorized users.