Working memory is imprecise, and these imprecisions can be explained by the combined influences of random diffusive error and systematic drift toward a set of stable states (“attractors”). However, the neural correlates of diffusion and drift remain unknown. Here, we investigated how delay-period activity in frontal and parietal cortex, which is known to correlate with the decline in behavioral memory precision observed with increasing memory load, might relate to diffusion and drift. We analyzed data from an existing experiment in which subjects performed delayed recall for line orientation, at different loads, during functional magnetic resonance imaging (fMRI) scanning. To quantify the influence of drift and diffusion, we modeled subjects’ behavior using a discrete attractor model and calculated within-subject correlation between frontal and parietal delay-period activity and whole-trial estimates of drift and diffusion. We found that although increases in frontal and parietal activity were associated with increases in both diffusion and drift, diffusion explained the most variance in frontal and parietal delay-period activity. In comparison, a subsequent whole-brain regression analysis showed that drift, rather than diffusion, explained the most variance in delay-period activity in lateral occipital cortex. These results are consistent with a model of the differential recruitment of general frontoparietal mechanisms in response to diffusive noise and of stimulus-specific biases in occipital cortex.