Species living in seasonal environments often adaptively time their reproduction in response to photoperiod cues. We characterized the expression of genes in the flowering-time regulatory network across wild populations of the common sunflower, Helianthus annuus, that we found to be adaptively differentiated for photoperiod response. The observed clinal variation was associated with changes at multiple hierarchical levels in multiple pathways. Paralogue-specific changes in FT homologue expression and tissue-specific changes in SOC1 homologue expression were associated with loss and reversal of plasticity, respectively, suggesting that redundancy and modularity are gene network characteristics easily exploited by natural selection to produce evolutionary innovation. Distinct genetic mechanisms contribute to convergent evolution of photoperiod responses within sunflower, suggesting regulatory network architecture does not impose strong constraints on the evolution of phenotypic plasticity.