Abstract The Milky Way’s dark matter halo is expected to host numerous low-mass subhalos with no detectable associated stellar component. Such subhalos are invisible unless their dark matter annihilates to visible states such as photons. One of the established methods for identifying candidate subhalos is to search for individual unassociated gamma-ray sources with properties consistent with the dark matter expectation. However, robustly ruling out an astrophysical origin for any such candidate is challenging. In this work, we present a complementary approach that harnesses information about the entire population of subhalos—such as their spatial and mass distribution in the Galaxy—to search for a signal of annihilating dark matter. Using simulated data, we show that the collective emission from subhalos can imprint itself in a unique way on the statistics of observed photons, even when individual subhalos may be too dim to be resolved on their own. Additionally, we demonstrate that, for the models we consider, the signal can be identified even in the face of unresolved astrophysical point-source emission of extragalactic and Galactic origin. This establishes a new search technique for subhalos that is complementary to established methods, and that could have important ramifications for gamma-ray dark matter searches using observatories such as the Fermi Large Area Telescope and the Cerenkov Telescope Array.