We determined how learning modifies neural representations in primary visual cortex (V1) during acquisition of a visually guided behavioral task. We imaged the activity of the same layer 2/3 neuronal populations as mice learned to discriminate two visual patterns while running through a virtual corridor, where one pattern was rewarded. Improvements in behavioral performance were closely associated with increasingly distinguishable population-level representations of task-relevant stimuli, as a result of stabilization of existing and recruitment of new neurons selective for these stimuli. These effects correlated with the appearance of multiple task-dependent signals during learning: those that increased neuronal selectivity across the population when expert animals engaged in the task, and those reflecting anticipation or behavioral choices specifically in neuronal subsets preferring the rewarded stimulus. Therefore, learning engages diverse mechanisms that modify sensory and non-sensory representations in V1 to adjust its processing to task requirements and the behavioral relevance of visual stimuli. •V1 neurons increasingly discriminate task-relevant stimuli with learning•Chronic imaging reveals single cell changes underlying this population effect•Learning-related changes are reduced when animals ignore task-relevant stimuli•Anticipatory and behavioral choice-related signals emerge in reward-predicting cells By tracking the same visual cortex neurons across days, Poort et al. demonstrate how learning a visual task leads to increasingly distinguishable representations of relevant stimuli. These changes parallel the emergence of diverse non-sensory signals in specific neuronal subsets.