Correlated dispersal paths between two or more individuals are widespread across many taxa. The population genetic implications of this collective dispersal have received relatively little attention. Here we develop two-sample coalescent theory that incorporates collective dispersal in a finite island model to predict expected coalescence times, genetic diversities, and F-statistics. We show that collective dispersal reduces mixing in the system, which decreases expected coalescence times and increases FST. The effects are strongest in systems with high migration rates. Collective dispersal breaks the invariance of within-deme coalescence times to migration rate, whatever the deme size. It can also cause FST to increase with migration rate because the ratio of within- to between-deme coalescence times can decrease as migration rate approaches unity. This effect is most biologically relevant when deme size is small. We find qualitatively similar results for diploid and gametic dispersal. We also demonstrate with simulations and analytical theory the strong similarity between the effects of collective dispersal and anisotropic dispersal. These findings have implications for our understanding of the balance between drift–migration–mutation in models of neutral evolution. This has applied consequences for the interpretation of genetic structure (e.g., chaotic genetic patchiness) and estimation of migration rates from genetic data.