The ability of mutations to facilitate adaptation to changing conditions is central to evolution. The T4 bacteriophage clamp-loader complex, an oligomeric AAA+ ATPase required for processive DNA replication, is normally highly tolerant to most mutations. To study the adaptive capacity of the clamp loader, we created a chimeric version in which the catalytic AAA+ modules are replaced by those from another phage, resulting in a ∼5000-fold reduction in phage replication rate. This fitness decrease is caused by a reduction in affinity between the clamp loader and the clamp. A directed-evolution experiment revealed that multiple substitutions to a single negatively-charged residue in the chimeric clamp loader - Asp 86 - restore fitness to within ∼20-fold of wildtype, most likely by removing an adventitious electrostatic repulsive interaction with the sliding clamp. Deep mutagenesis shows that reduced fitness of the chimeric clamp loader is compensated for by lysine and arginine substitutions of several DNA-proximal residues in the clamp loader or the sliding clamp. Our results demonstrate that there is a latent capacity for increasing affinity of the clamp loader for DNA and the sliding clamp, such that even single point mutations can readily compensate for the loss of function due to suboptimal interactions elsewhere.