Given the unique spatial structure of stream habitat and the stochasticity characteristic of lotic ecosystems, metacommunity approaches hold much promise in the field of stream ecology. We take advantage of the tight parallels between neutral theories of molecular evolution and community assembly and present a novel conceptual approach to evaluating the role of stochasticity and dispersal limitation in structuring stream metacommunities. The analogous neutral frameworks generate similar expectations for the spatial structure of species comprising communities and genes comprising populations, particularly among patchily distributed, isolated local habitats (e.g., headwater streams) where among-stream dispersal is expected to be limited. Our emphasis is on the conceptual value of this approach, but we also used a limited data set composed of intensively sampled community and population-genetic data collected from 5 to 7 Rocky Mountain alpine streams for illustrative purposes. We characterized neutral population genetic structure as mitochondrial haplotype distributions for the blackfly Prosimulium neomacropyga, which shows strong genetic isolation by distance across the study region. We assessed community structure as the relative frequencies of ecologically similar species in the family Chironomidae collected annually over 2000–2003. Species richness was positively correlated with haplotype richness across streams (r  =  0.55), and analogous methods revealed significant β diversity at both the population-genetic (F_ST  =  0.23) and the community (F_ST  =  0.16) levels. However, a more spatially explicit comparison of pairwise community dissimilarity and genetic distance revealed no evidence of correlation (Mantel test, r  =  −0.18, p  =  0.54), a result suggesting no effect of spatial distance on community similarity at the relatively fine spatial scale of our study. We discuss 2 key arguments to explain the lack of community distance decay: 1) unaccounted environmental differences among streams, and 2) varying spatial and temporal scales of neutral processes (including genetic drift and ecological drift; i.e., stochastic temporal change) between population-genetic and community levels. Evidence for both selective and neutral explanations is compelling in this system. The explanations cannot be disentangled with the current data, but the study has strong heuristic value that we hope will stimulate future efforts in stream metacommunity analysis.