Mothers often provide much of the early environment for their offspring. These maternal effects are predicted to result in unusual evolutionary dynamics in offspring traits if they are themselves heritable, but these important predictions have not previously, to our knowledge, been tested in the wild. Here, we quantified the responses of red squirrels (Tamiasciurus hudsonicus) to documented episodes of natural selection and found support for both of the fundamental predictions of models that describe maternal effect evolution. First, changes in juvenile growth rates across one generation of selection were five times greater than predicted by heritability (h2) alone, but were consistent with the additional contribution of maternal genetic effects. Second, responses to selection were influenced not only by the strength of selection in the current generation, but also by selection in the previous generation, indicating the presence of evolutionary momentum. These results were in agreement with predictions of a simple model including litter size as the only maternal effect, and provide, to our knowledge, the first empirical evidence for the importance of maternal effects to evolutionary dynamics in a natural population.