Diverse computations in the neocortex are aided by specialized GABAergic interneurons (INs), which selectively target other INs. However, much less is known about how these canonical disinhibitory circuit motifs contribute to network operations supporting spatial navigation and learning in the hippocampus. Using chronic two-photon calcium imaging in mice performing random foraging or goal-oriented learning tasks, we found that vasoactive intestinal polypeptide-expressing (VIP+), disinhibitory INs in hippocampal area CA1 form functional subpopulations defined by their modulation by behavioral states and task demands. Optogenetic manipulations of VIP+ INs and computational modeling further showed that VIP+ disinhibition is necessary for goal-directed learning and related reorganization of hippocampal pyramidal cell population dynamics. Our results demonstrate that disinhibitory circuits in the hippocampus play an active role in supporting spatial learning. Display omitted •Ca2+ imaging indicates bimodal activity dynamics of VIP interneurons in vivo•Activity of VIP interneurons is modulated by task and learning demands•VIP-mediated disinhibition supports spatially guided reward learning Turi et al. imaged activity of VIP-expressing interneurons of hippocampal area CA1 in vivo. They show learning-related reorganization in VIP population dynamics. VIP interneurons provide behavioral state-dependent disinhibition for CA1 pyramidal cells that supports spatial reward learning.