Recent work has shown that evolvability plays a key role in determining the long-term population dynamics of asexual clones. However, simple considerations suggest that the evolvability of a focal lineage of bacteria should also be influenced by the evolvability of its competitors. First, evolvable competitors should accelerate evolution by impeding the fixation of the focal lineage through a clonal interference–like mechanism. Second, evolvable competitors should increase the strength of selection by rapidly degrading the environment, increasing selection for adaptive mutations. Here we tested these ideas by allowing a high-fitness clone of the bacterium Pseudomonas aeruginosa to invade populations of two low-fitness resident clones that differ in their evolvability. Both competition from mutations in the resident lineage and environmental degradation lead to faster adaptation in the invader through fixing single mutations with a greater fitness advantage. The results suggest that competition from mutations in both the successful invader and the unsuccessful resident shapes the adaptive trajectory of the invader through both direct competition and indirect environmental effects. Therefore, to predict evolutionary outcomes, it will be necessary to consider the evolvability of all members of the community and the effects of adaptation on the quality of the environment. This is particularly relevant to mixed microbial communities where lineages differ in their adaptive potential, a common feature of chronic infections.