Despite substantial progress in cancer therapy in recent decades, patients with cancer remain at high suicide risk. Data from individual studies have not been comprehensively quantified and specific risk factors are ill-defined. We assessed suicide mortality risk according to cancer prognosis, stage, time since diagnosis, gender, ethnicity, marital status, year of recruitment and geographic region. We searched EMBASE, MEDLINE, PsycINFO, Web of Science, CINAHL and Google Scholar for relevant articles up to February 2021. We used a random effects model, performed meta-regression meta-analysis and assessed heterogeneity and publication bias using I², funnel plots and Egger’s and Begg’s tests. We performed a systematic review including 62 studies and 46,952,813 patients. To avoid patient sample overlap, the meta-analysis was performed on 28 studies, involving 22,407,690 patients with cancer. Suicide mortality was significantly increased compared with the general population (standardized mortality ratio = 1.85, 95% confidence interval = 1.55–2.20). Risk was strongly related to cancer prognosis, cancer stage, time since diagnosis and geographic region. Patients with cancer, particularly those with specific risk factors, should be closely monitored for suicidality and need specialized care to reduce short- and long-term risks of suicide.