People must constantly select among potential thoughts and actions in the face of competition from (a) multiple task-relevant options (underdetermined competition) and (b) strongly dominant options that are not appropriate in the current context (prepotent competition). These types of competition are ubiquitous during language production. In this work, we investigate the neural mechanisms that allow individuals to effectively manage these cognitive control demands and to quickly choose words with few errors. Using fMRI, we directly contrast underdetermined and prepotent competition within the same task (verb generation) for the first time, allowing localization of the neural substrates supporting the resolution of these two types of competition. Using a neural network model, we investigate the possible mechanisms by which these brain regions support selection. Together, our findings demonstrate that all competition is not alike: resolving prepotent competition and resolving underdetermined competition rely on partly dissociable neural substrates and mechanisms. Specifically, activation of left ventrolateral pFC is specific to resolving underdetermined competition between multiple appropriate responses, most likely via competitive lateral inhibition. In contrast, activation of left dorsolateral pFC is sensitive to both underdetermined competition and prepotent competition from response options that are inappropriate in the current context. This region likely provides top–down support for task-relevant responses, which enables them to out-compete prepotent responses in the selection process that occurs in left ventrolateral pFC.