Suicidal behavior is highly prevalent in major depressive disorder (MDD), though not present in all patients. It is unclear whether the tendency for suicidal behavior is associated with a unique functional neuroanatomical signature identifiable through neuroimaging. In this study, we investigated brain activation in suicidal and non-suicidal patients with MDD during facial emotion processing and executive control. Functional magnetic resonance imaging (fMRI) data from the NESDA-fMRI study (MDD patients N = 103, healthy controls N = 26, HC) were analyzed. Patients were divided in a group of suicide attempters (N = 18, SA), suicide ideators (N = 31, SI) and a patient-control group (N = 73, PC). A gender discrimination task with emotional faces and the Tower of London executive planning task were investigated. An ANOVA was performed to compare brain activation among suicidal patients (SA + SI), PC and HC first and then among SI, SA, PC and HC. Significance was determined as meeting p <.05 family wise error (FWE) corrected at the voxel-level. We observed that SA patients showed lower activation in the bilateral fusiform gyri during emotional faces processing compared to SI, PC and HC. No group differences were found during executive planning. Results were independent of childhood emotional maltreatment, depression severity, anxiety severity, use of psychotherapy and SSRI-use. Results suggest that a propensity for suicidal behavior in MDD is associated with abnormal emotional processing but not executive functioning, represented by altered face processing compared to non-suicidal patients and controls. While in need of replication, these results indicate that altered fusiform gyrus activation during emotion processing may serve as a marker for suicidality.