How underlying mechanisms bias evolution toward predictable outcomes remains an area of active debate. In this study, we leveraged phenotypic plasticity and parallel adaptation across independent lineages of Trinidadian guppies (Poecilia reticulata) to assess the predictability of gene expression evolution during parallel adaptation. We observed substantial gene expression plasticity as well as the evolution of expression plasticity itself across populations. Genes exhibiting expression plasticity within populations were more likely to also differ in expression between populations, with the direction of expression divergence more likely to be opposite than in the same direction as plasticity. While we also found more overlap than expected by chance in genes differentially expressed between high- and low-predation populations from different lineages, the majority of differentially expressed genes were not shared between distinct evolutionary lineages. Our data suggest alternative transcriptional configurations associated with shared phenotypes, highlighting a role for transcriptional flexibility associated with parallel phenotypic evolution in a species known for rapid adaptation.