Environmental variables, such as resource quality, shape growth in organisms, dictating body size, an important correlate of fitness. Variation in prey characteristics among populations is frequently associated with similar variation in predator body sizes. Anthropogenic alterations to prey landscapes impose novel ecological pressures on predators that may shift predator phenotypes. Research has focused on determining the adaptability of the phenotypic response by testing its genetic heritability. Here, we asked if anthropogenic shifts in prey size across the landscape correlate with juvenile growth rates among populations of watersnakes with divergent life-history phenotypes. We sought to determine if growth rate variation is the product of genetic adaptation or a non-heritable phenotypic response. Using a common-garden design, we measured growth of neonate snakes from fish farms varying in prey size. We found juvenile growth rates are faster for snakes with larger initial body sizes and from populations with larger average prey sizes. Our data suggest variability in juvenile grow rates within and among populations are not the product of genetic adaptation, but the indirect consequence of initial offspring size variation and prey consumption. We propose larger offspring sizes may favor increased juvenile growth rates, mediated through a larger morphological capacity to consume and process energy resources relative to smaller individuals. This experiment provides evidence supporting the growing body of literature that non-heritable responses may be significant drivers of rapid phenotypic divergence among populations across a landscape. This mechanism may explain the stability and colonization of populations in response to rapid, human-mediated, landscape changes.