The contents of working memory (WM) steer visual attention, but the extent of this guidance can be strategically enhanced or inhibited when WM content is reliably helpful or harmful to a visual task. Current understanding of the neural substrates mediating the cognitive control over WM biases is limited, however, by the correlational nature of functional MRI approaches. A recent fMRI study provided suggestive evidence for a functional lateralization of these control processes in posterior parietal cortex (PPC): activity in left PPC correlated with the presentation of WM cues that ought to be strategically enhanced to optimize performance, while activity in the right PPC correlated with the presentation of cues that ought to be inhibited to prevent detrimental attentional biases in a visual search. Here, we aimed to directly assess whether the left and right PPC are causally involved in the cognitive control of WM biases, and to clarify their precise functional contributions. We therefore applied 1 Hz repetitive transcranial magnetic stimulation (rTMS) to left and right PPC (and a vertex control site) prior to administering a behavioral task assessing WM biasing control functions. We observed that the perturbation of left PPC eliminated the strategic benefit of predictably helpful WM cueing, while the perturbation of right PPC amplified the cost of unpredictable detrimental WM cueing. The left and right PPC thus play distinct causal roles in WM-attention interactions: the left PPC to maximize benefits, and the right PPC to minimize costs, of internally maintained content on visual attention.