Automatic imitation--the unintended copying of observed actions--is thought to be a behavioral product of the mirror neuron system (MNS). Evidence that the MNS develops through associative learning comes from previous research showing that automatic imitation is attenuated by countermirror training, in which the observation of one action is paired contingently with the execution of a different action. If the associative account of the MNS is correct, countermirror training should show context specificity, because countermirror associations render action stimuli ambiguous, and ambiguity promotes contextual control. Two experiments that confirm this prediction are reported. In Experiment 1 we found less residual automatic imitation when human participants were tested in their countermirror training context. In Experiment 2, sensorimotor training where participants made action responses to novel abstract stimuli was insensitive to the same context manipulation, confirming that the former result was not a procedural artifact. Contextual modulation may enable the MNS to function effectively in spite of the fact that action observation often excites multiple conflicting MNS responses. (Contains 6 figures and 2 tables.)