A major challenge in microbial evolutionary ecology is to understand how fitness-related traits vary in natural populations of microorganisms at defined spatial scales and subsequently to identify the forces that maintain such variation. The Gram-negative soil bacterium Myxococcus xanthus is a model system for the study of gliding motility, which is driven by two complementary motility systems in this species and is central to its social lifestyle. We tested whether the ecological context of a centimetre-scale M. xanthus population allows the coexistence of diverse motility-related phenotypes. Swarming rates among 26 clones isolated at the centimetre scale were found to vary greatly in multiple laboratory environments. This variation appears to be motility-specific, as it is not explained by a correlated variation in intrinsic growth rate. In contrast to the common reference strain DK1622, most isolates swarmed faster on hard agar than on soft agar, highlighting the difficulty of inferring species characteristics from laboratory reference strains. These isolates also varied greatly in swarm morphology and in the effect of nutrient limitation on swarming rate. Our results show that diverse swarming phenotypes can coexist in a small-scale bacterial population.