Two fundamental unsolved problems in evolutionary biology are (1) predicting how genotype and environment interact to shape evolutionary processes and (2) elucidating the mechanisms by which genetic and environmental influences produce well-adapted phenotypes. Central to these questions are contrasting views on how environmentally induced variation (phenotypic plasticity) influences adaptive evolution, and how selection in a novel environment acts on multiple, mechanistically linked traits. Are systems flexible, such that there are multiple possible mechanistic ‘solutions’ that can give rise to a certain phenotype, or are systems constrained such that solutions are limited? To address this question, we take advantage of the Trinidadian guppy system to examine genetic and environmental influences on gene expression and behavior. We find that both genetic background and rearing environment alter correlations among behaviors and between gene expression and behavior. We propose that this flexibility may help maintain favorable trait constellations across different environments and perhaps contribute to guppies’ ability to rapidly adapt to changing environmental pressures.