Phenotypic evolution in animals is constrained by the mechanics of early development. How do major transitions in development occur? Historically, efforts to address this question have been limited to comparative methods. The polychaete annelid Streblospio benedicti provides a unique opportunity to use forward genetics to experimentally dissect a major transition in animal development. S. benedicti is ideal because it produces two distinct offspring types that differ in egg size, early development, and larval morphology. S. benedicti is thus a genetic model for the evolutionarily common transition between indirect and direct development. Using genetic crosses between these types, we constructed the first annelid genetic map, which reveals the distribution of genetic factors affecting a suite of genetically separable developmental phenotypes. Because early development is strongly influenced by maternal effects, our cross design disentangles maternal and zygotic genetic effects and shows that a transition from indirect to direct development requires contributions from both the zygotic and maternal genome; an increase in egg size alone is not sufficient to change development mode. By identifying the loci responsible for regulating early development, we uncover how the dimorphic developmental program is determined on a whole-genome level.