Ligand-induced transcription relies on enhancer clusters, but what keeps these regulatory hubs primed for rapid activation? In estrogen-responsive genes, enhancer clusters are swiftly decorated by estrogen receptor-alpha (ERα) within minutes of ligand stimulation, far too fast for traditional chromatin remodelling, suggesting they are maintained in a poised state by unknown factors. Yet, this activation is transient: ERα-bound clusters lose their strength as ERα dissociates approximately three hours post-stimulation, raising a fundamental question—how do these clusters remain accessible between successive cycles of estrogen signaling, such as those occurring during the menstrual cycle? Here, we reveal a surprising mechanism: in the absence of ERα at the end of signaling, the androgen receptor (AR) steps in as a placeholder, primarily occupying estrogen response elements (EREs) and, to a lesser extent, AR and FOXA1 binding sites. This placeholder function is mediated by direct DNA binding, as mutations in AR’s DNA-binding domain abolish its recruitment. Strikingly, when AR is unable to bind, FOXA1 floods these enhancer clusters, dramatically increasing chromatin activity and priming them for even stronger ERα binding in the next round of estrogen stimulation. This suggests that AR passively maintains enhancer clusters in an optimal poised state, preventing excessive FOXA1-driven enhancer reprogramming, an event linked to transcriptional rewiring in breast cancer cells. Our findings redefine enhancer regulation, revealing a dynamic interplay between transcription factors that safeguard enhancer clusters between signaling cycles. By demonstrating functional redundancy at these regulatory elements, we challenge the conventional separation between pioneering factors and transcription factors, shedding new light on how enhancer landscapes are maintained and reshaped over time.