Evolvability-the capacity to generate adaptive variation-is a trait that can itself evolve through natural selection. However, the idea that mutation can become biased toward adaptive outcomes remains controversial. In this work, we report the evolution of enhanced evolvability through localized hypermutation in experimental populations of bacteria. The evolved mechanism is analogous to the mutation-prone sequences of contingency loci observed in pathogenic bacteria. Central to this outcome was a lineage-level selection process, where success depended on the capacity to evolve between two phenotypic states. Subsequent evolution showed that the hypermutable locus is itself evolvable with respect to alterations in the frequency of environmental change. Lineages with localized hypermutability were more likely to acquire additional adaptive mutations, revealing an unanticipated benefit.