Urbanized harbors and embayments scattered along marine shorelines act as important sources of a wide range of chemical contaminants, which include metallic trace elements (MTE). Within the semi-enclosed Mediterranean Sea, the high number of such areas might locally challenge the persistence of coastal marine species. In recent decades, biomonitoring studies, using sentinel species such as mussels, have increased knowledge of coastal contamination and provided a number of contentious potential environmental surveillance biomarkers, which contributed to a better comprehension toward the acclimation abilities of marine organisms, to actual anthropogenically derived environments. The aim of this study was to characterize the influence of the chemically, multi-contaminated, Bay of Toulon (France) on the young fauna, using juvenile sea urchins Paracentrotus lividus as a proxy. Hatchery-produced individuals were immersed, for 1 mo, within the bay, at four contrasted sites for MTE concentrations. At the end of the experiment, growth and transcript abundances of key genes, involved in the acclimation process, were assessed. Contrasted phenotypic and molecular responses were observed evidencing a significant environmental influence. Specifically, under the high metallic stress, a dwarfing response was observed, associated with a high level of metallothionein and a low level of hsp response. In addition, the level of DNA methyltransferase transcript abundance was inversely correlated with the level of MTE concentrations, highlighting that the chronic exposure to metallic contaminants would probably increase the risk of genetic mutations, such as those consecutive to transpositions. Overall, this study indicates that further in-depth research into the mechanisms driving plasticity and adaptive changes at the population level is required.