Much thought has been given to the individual-level traits that may make a species a successful colonizer. However, these traits have proven to be weak predictors of colonization success. Here, we test whether population-level characteristics, specifically genetic diversity and population density, can influence colonization ability on a short-term ecological timescale, independent of longer-term effects on adaptive potential. Within experimentally manipulated populations of the weedy herb Arabidopsis thaliana, we found that increased genetic diversity increased colonization success measured as population-level seedling emergence rates, biomass production, flowering duration, and reproduction. Additive and non-additive effects contributed to these responses, suggesting that both individual genotypes (sampling effect) and positive interactions among genotypes (complementarity) contributed to increased colonization success. In contrast, manipulation of plant density had no effect on colonization success. The heightened ability of relatively genetically rich populations to colonize novel habitats, if a general phenomenon, may have important implications for predicting and controlling biological invasions.