Dispersal is key to understanding ecological and evolutionary dynamics. Dispersal may itself evolve and exhibit phenotypic plasticity. Specifically, organisms may modulate their dispersal rates in response to the density of their conspecifics (density-dependent dispersal) and their own sex (sex-biased dispersal). While optimal dispersal plastic responses have been derived from first principles, the genetic and molecular basis of dispersal plasticity has not been modelled. An understanding of the genetic architecture of dispersal plasticity is especially relevant for understanding dispersal evolution during rapidly changing spatial ecological conditions such as range expansions. In this context, we develop an individual-based metapopulation model of the evolution of density-dependent and sex-biased dispersal during range expansions. We represent the dispersal trait as a gene-regulatory network (GRN), which can take population density and an individual's sex as an input and analyse emergent context- and condition-dependent dispersal responses. We compare dispersal evolution and ecological dynamics in this GRN model to a standard reaction norm (RN) approach under equilibrium metapopulation conditions and during range expansions. We find that under equilibrium metapopulation conditions, the GRN model produces emergent density-dependent and sex-biased dispersal plastic response shapes that match the theoretical expectation of the RN model. However, during range expansion, when mutation effects are large enough, the GRN model leads to faster range expansion because GRNs can maintain higher adaptive potential. Our results imply that, in order to understand eco-evolutionary dynamics in contemporary time, the genetic architecture of traits must be taken into account.