To behave adaptively in complex environments, animals must selectively process the most important information in space while ignoring distractors. Here, we report that an evolutionarily ancient group of brainstem inhibitory neurons, called PLTi, is surprisingly critical for this function of selective spatial attention. In freely behaving mice performing a human-like spatial attention task, we found that bilateral silencing of PLTi severely disrupted target selection without causing perceptual or task-relevant motor impairments. PLTi’s effects depended necessarily on goal-relevant, rather than just physical salience-based signals, together revealing it as a specialized site for priority-driven attentional target selection. PLTi’s core contribution was in controlling accuracy and categorical precision of the decision boundary separating the target from lower-priority distracters. PLTi’s control of neural representations of competing stimuli in the superior colliculus, an established attentional hub, revealed a potential mechanistic pathway. PLTi may, therefore, be a conserved brainstem site across vertebrates for winner-take-all-like spatial decisions.