Food allergy is a complex immune-mediated condition that can affect multiple organ systems, including the brain. We have previously demonstrated that hypersensitization of healthy, wild-type male mice to a cow’s milk allergen, β-lactoglobulin (BLG), that significantly increases the levels of immunoglobulin E antibody against the allergen (BLG-IgE), results in neurobehavioral pathologies without observable allergic reactions. However, underlying molecular mechanisms remain poorly understood. To identify immune factors that mediate, and can potentially be used to detect, neurobehavioral pathologies caused by food allergy, we analyzed plasma cytokine profiles and examined their correlation with BLG-IgE levels and behavioral changes in male and female mice. The marble-burying test and the novel-object recognition test were used for the assessment of innate behavior and cognitive function. BLG-IgE correlated with 9 (23%) male and 8 (20%) female cytokines, with 4 (10%) shared (positive except TNF RII). Marble-burying correlated with 12 (31%) male, 6 (15.4%) female, and 4 (10%) shared (negative except bFGF, IL21 and TNF RII); cognition correlated negatively with 19 (50%) male cytokines; positive IL-21 in females. Seven cytokines (CXCL13, Eotaxin, Eotaxin2, ICAM-1, IL-1a, MCP-1, TNF RI) were significantly correlated with BLG-IgE levels and behavioral changes. Despite no behavioral alterations, female cytokines correlated with marble-burying. The predominance of cytokine associations in males supports a stronger systemic immune-behavioral relationship. Cytokine-behavior associations in females suggest that circulating immune signatures may capture subtle neuroimmune changes not appear in behavioral outcomes. Together, these findings identify sex-specific circulating cytokine biomarkers associated with subclinical sensitization and behavioral outcomes in chronic food allergy.