The degree of plasticity an individual expresses when moving into a new environment is likely to influence the probability of colonization and potential for subsequent evolution. Yet few empirical examples exist where the ancestral and derived conditions suggest a role for plasticity in adaptive genetic divergence of populations. Here we explore the genetic and plastic components of shoaling behaviour in two pairs of populations of Poecilia reticulata (Trinidadian guppies). We contrast shoaling behaviour of guppies derived from high- and low-predation populations from two separate drainages by measuring the shoaling response of second generation laboratory-reared individuals in the presence and absence of predator induced alarm pheromones. We find persistent differences in mean shoaling cohesion that suggest a genetic basis; when measured under the same conditions high-predation guppies form more cohesive shoals than low-predation guppies. Both high and low-predation guppies also exhibit plasticity in the response to alarm pheromones, by forming tighter, more cohesive shoals. These patterns suggest a conserved capacity for adaptive behavioural plasticity when moving between variable predation communities that are consistent with models of genetic accommodation.