Acclimatization through phenotypic plasticity represents a more rapid response to environmental change than adaptation and is vital to optimize organisms’ performance in different conditions. Generally, animals are less phenotypically plastic than plants, but reef-building corals exhibit plant-like properties. They are light-dependent with a sessile and moddular construction that facilitates rapid morphological changes within their lifetime. We induced phenotypic changes by altering light exposure in a reciprocal transplant experiment and found that coral plasticity is a colony trait emerging from comprehensive morphological and physiological changes within the colony. Plasticity in skeletal features optimized coral light harvesting and utilization and paralleled with significant methylome and transcriptome modifications. Network-associated responses resulted in the identification of hub genes and clusters associated to the change in phenotype: inter-partner recognition and phagocytosis, soft tissue growth and biomineralization. Furthermore, we identified hub genes putatively involved in animal photoreception-phototransduction. These findings fundamentally advance our understanding of how reef-building corals repattern the methylome and adjust a phenotype, revealing an important role of light sensing by the coral animal to optimize photosynthetic performance of the symbionts. Overall design: To examine the phenotype to methylome association, we conducted a reciprocal transplant experiment to induce light-mediated phenotypic responses in the reef-building Elkhorn coral Acropora palmata and investigated DNA methylation and transcriptional responses potentially responsible for plasticity. Extensive biometrics revealed not only changes in coral tissue pigmentation and metabolic rates but also in skeletal morphology after five weeks. This skeletal remodeling was accompanied by intragenic methylome repatterning, discovered by signal detection with machine learning-based analysis. We further integrated differentially methylated (DMG) and expressed (DEG) gene datasets to elucidate how light responses integrate into gene regulatory networks controlling functional traits. By exploring the resulting hub genes and gene clusters, we were able to predict functional associations with observed phenotype changes and identify markers of plasticity in reef-building corals. Moreover, our results contribute to emerging evidence that epigenetics contribute to the machinery that can alter DNA structure during skeletal remodeling in metazoans. To induce phenotypic plasticity, we performed a reciprocal transplant experiment. We sampled 3 colonies (representing 3 distinct multilocus genotypes, or genets, as detected with Standard Tools for Acroporid Genotyping STAGdb) from a depth of 2-3 m, each at least 300 m apart. We collected ~7 cm2 fragments from HL (n= 42 Upperside) and LL (n = 42 Underside) surfaces of branch surfaces keeping track of genet identification. We settled them in a reef-deployed PVC structure designed to simulate the light condition and colony position of source colonies. We placed all coral fragments in their original light condition and orientation (i.e. HL Uppersides facing up) and allowed them to heal and acclimate. Subsequently, we randomly divided HL fragments into control (Upperside Control) and treatment groups (Upperside Treatment), equal grouping was done for LL fragments (Underside Control and Underside Treatment). To induce phenotypic plasticity, coral fragments in treatment groups were flipped to the opposite light condition and position (i.e. high light fragments were flipped to a low light condition, while LL fragments were flipped to a HL position). This second acclimatory period was carried out for 5+ weeks. Four group conditions were analyzed after 13+ weeks of experiment: HL controls (n= 21 Upperside Control), HL?LL treatments (High Light to Low Light, n = 21, Upperside Treatment), LL controls (n= 21 Underside Control), LL?HL treatments (Low Light to High Light, n = 21, Underside Treatment)).