In order to understand (re-)colonization of microhabitats and bacterial succession in soil, it is important to understand which members of soil bacterial communities are most motile in the porous soil matrix. To address this issue, we carried out a series of experiments in sterilized soil microcosms. Using two different model strains, Pseudomonas fluorescens strain Pf0–1 and Collimonas fungivorans strain Ter331, we first determined the influence of nutrient availability on bacterial expansion rates. Based on these results, we then conducted similar microcosm experiments to examine microbial mobility within natural soil bacterial communities under a single nutrient regime. The expansion of bacterial populations within the community was assayed by quantitative PCR and pyrosequencing of 16S rRNA gene fragments. We observed that only a relatively small subset of the total community was able to expand to an appreciable distance (more than 2 cm) within 48 hours, with the genera Undibacterium, Pseudomonas, and Massilia and especially the family Enterobacteriaceae dominating the communities more distant from the point of inoculation. These results suggest that (re-)colonization of open habitats in soil may be dominated by a few rapidly moving species, which may have important consequences for microbial succession.