Models of “plasticity-first” evolution are attractive because they explain the rapid evolution of new complex adaptations. Nev- ertheless, it is unclear whether plasticity can facilitate rapid microevolutionary change between diverging populations. Here, we show how plasticity may have generated adaptive differences in fecundity between neighboring wild populations of burying bee- tles Nicrophorus vespilloides. These populations occupy distinct Cambridgeshire woodlands that are just 2.5 km apart and that probably originated from a common ancestral population about 1000-4000 years ago. We find that populations are divergently adapted to breed on differently sized carrion. Adaptive differences in clutch size and egg size are associated with divergence at loci connected with oogenesis. The populations differ specifically in the elevation of the reaction norm linking clutch size to carrion size (i.e., genetic accommodation), and in the likelihood that surplus offspring will be lost after hatching. We suggest that these two processes may have facilitated rapid local adaptation on a fine-grained spatial scale.