Sources of variation in growth in body mass were assessed in natural and experimental conditions of high and low food abundance using reciprocal cross-fostering techniques and long-term data (1987–2002) for a population of North American red squirrels (Tamiasciurus hudsonicus). Growth rates were significantly higher in naturally good and food supplemented conditions, than in poor conditions. Mother–offspring resemblance was higher in poor conditions as a result of large increases in both the direct genetic variance and direct-maternal genetic covariance and a smaller increase in the coefficient of maternal variation. Furthermore, the genetic correlation across environments was significantly less than one indicating that sources of heritable variation differed between the two environments. These results are consistent with the hypothesis that selection has eroded heritable variation for growth more in good conditions and indicate the potential for independent adaptation of growth rates in good and poor conditions.