Background <p>Suicidal ideation and behaviour are major global mental health issues and leading causes for mortality. While existing evidence indicates brain functional deficits of suicidal thoughts and behaviours, the neural underpinnings of these deficits remain unclear, possibly due to various sources of methodological heterogeneities.</p> Methods <p>We conducted a pre-registered meta-analysis including 22 task-based functional magnetic resonance imaging studies that compared suicidal individuals (<i>N</i> = 459, 63.83% females) with non-suicidal psychiatric controls (<i>N</i> = 681, 52.72% females). Separate analyses were conducted in the emotion and non-emotion (cognitive and risky decision making) domains. Subgroup and meta-regression analyses addressed methodological heterogeneities including patient diagnosis, suicidal characteristics (ideation vs. behaviours) and task type.</p> Results <p>In emotion tasks, general suicidality (pooling across ideation and behaviours) and suicidal behaviours were both associated with hyperactivities in the left sensorimotor cortices and hippocampus/parahippocampus, alongside hypoactivity in the bilateral visual cortices. However, only the hypoactivity among visual areas was consistently replicated in all subgroup analyses. In non-emotion tasks, general suicidality and suicidal behaviours were both associated with hyperactivity in the left precentral gyrus and the right middle temporal gyrus, which were consistently replicated in all subgroup analyses. Meta-regression analyses further identified larger suicidality-associated functional changes in frontotemporal regions in studies with higher female proportions, and in hippocampal and temporal regions in studies with older participants.</p> Conclusions <p>Our findings indicate that the blunted perceptual emotion processing and heightened motor system reactivity are key neural features of suicidality, which provide potential neural targets for interventions on suicidal individuals.</p>