Type I interferon IFNβ is a key regulator of the immune response, and its dysregulated expression causes disease. The regulation of IFNβ promoter activity has been a touchpoint of mammalian gene control research since the discovery of functional synergy between two stimulus-responsive transcription factors (TFs) nuclear factor kappa B (NFκB) and interferon regulatory factors (IRF). However, subsequent gene knockout studies revealed that this synergy is condition-dependent such that either NFκB or IRF activation can be dispensable, leaving the precise regulatory logic of IFNβ transcription an open question. Here, we developed a series of quantitative enhancer states models of IFNβ expression control and evaluated them with stimulus-response data from TF knockouts. Our analysis confirmed that TF synergy is a hallmark of the regulatory logic but that it need not involve NFκB, as synergy between two adjacent IRF dimers is sufficient. We found that a sigmoidal binding curve at the distal site renders the dual IRF synergy mode ultrasensitive, allowing it only in conditions of high IRF activity upon viral infection. In contrast, the proximal site has high affinity and enables expression in response to bacterial exposure through synergy with NFκB. However, its accessibility is controlled by the competitive repressor p50:p50, which prevents basal IRF levels from synergizing with NFκB, such that NFκB-only stimuli do not activate IFNβ expression. The enhancer states model identifies multiple synergy modes that are accessed differentially in response to different immune threats, enabling a highly stimulus-specific but also versatile regulatory logic for stimulus-specific IFNβ expression.