Information in working memory is remarkably resilient to distraction. Yet, recent evidence suggests that distractors containing task-relevant features can disrupt working memory by inducing subtle biases in mnemonic representations. With multivariate decoding of human electroencephalography recordings, we show that temporally unpredictable distractors produce spatially-antagonistic mnemonic biases, across the visual hemifields. Grating distractors produced either an attractive or a repulsive mnemonic bias – a shift in the neural representation of the memorandum toward or away from the distractor’s orientation – depending, respectively, on whether the distractor appeared in the same hemifield as the memorandum, or opposite to it. Behavioral biases closely tracked these neural effects. We devised a two-tier ring attractor model with cross-hemifield inhibition, which comprehensively explains how the distractor’s timing, encoding strength, and input gating control these mnemonic biases. Our results provide a mechanistic account of distractor-induced biases, across space and time, in visual working memory.Lay SummaryWorking memory – the capacity to momentarily store important items or events – is remarkably robust to distraction. Yet, when a salient distractor with features resembling the memorized items appears, it can subtly alter (bias) working memory. Applying state-of-the-art neural decoding to human electrophysiological data, we show the such distractor biases are space-specific. The neural memory representation begins to resemble the distractor (attractive bias) when the distractor appears at the same location as the memory items, but becomes less like the distractor (repulsive bias) when the distractor appears further away. We tie together these experimental findings with a simple, computational model. The findings enhance our understanding of neural mechanisms underlying working memory and may be relevant for cognitive therapies addressing memory deficits.