In many animal species, the amount of care provided by parents is determined through a complex interaction of offspring signals and responses by parents to those signals. As predicted by honest signaling theory, we show that in the burrower bug, Sehirus cinctus, maternal provisioning responds to experimental manipulations of offspring condition. Despite this predicted environmental influence, we find evidence from two cross-foster experiments that variation in maternal care also stems from two distinct genetic sources: variation among offspring in their ability to elicit care and variation among parents in their response to offspring signals. Furthermore, as predicted by maternal-offspring coadaptation theory, offspring signaling is negatively genetically correlated with maternal provisioning.