Prior studies suggest that hypothalamic-pituitary-adrenal (HPA) axis stress response is a relatively stable risk factor for suicidal behavior in adults, and also that fluctuations in developmentally salient social stress (i.e., peer stress) predict acute suicidal ideation and behavior in adolescent females. Here, we test the hypothesis that periods of high peer stress are prospectively associated with concurrent episodes of suicidal ideation and behavior, but that abnormal cortisol responses to stress at baseline act as a diathesis that strengthens this stressor-suicidality link, using a longitudinal, multi-wave study design. We measured cortisol responses to an adolescent modification of the Trier Social Stress Test in 220 adolescent females recruited for mental health concerns, and measured stress (peer, academic, and mother-child) and suicidal ideation and behaviors repeatedly across 18 months. Logistic multilevel models revealed the predicted interaction between altered cortisol response and elevated periods of peer stress in predicting suicidal behavior, but not ideation. Higher-than-usual peer stress predicted suicidal ideation regardless of HPA function, but predicted suicide attempt only among those with blunted cortisol responses. Results suggest that peer stress serves to trigger suicidal ideation among female youth, but only triggers suicidal behavior among those with blunted cortisol reactivity.