Polyembryonic development is a unique mode of metazoan development in which a single zygote generates multiple embryos by clonal proliferation. The polyembryonic parasitic insect Copidosoma floridanum shows one of the most extreme cases of polyembryony, producing up to 2,000 embryos from a single egg. In addition, this wasp exhibits an unusual polyphenism, producing two morphologically distinct larval castes, termed precocious and reproductive, that develop clonally from the same zygote. This form of development seems incompatible with a model of insect development in which maternal pre-patterning of the egg specifies embryonic axial polarity. Here we show that maternal pre-patterning in the form of germ plasm creates cellular asymmetry at the four-cell stage embryo of Copidosoma that is perpetuated throughout development. Laser ablations of cells show that the cell inheriting the germ plasm regulates both the fate and proliferation of the reproductive caste. Thus, we have uncovered a new mechanism of caste specification, mediated by the regulatory capacity of a single cell. This study shows that the evolution of mammalian-like regulative development of an insect embryo relies on a novel cellular context that might ultimately enhance developmental plasticity.