Erythropoiesis-stimulating agents (ESAs) reduce anemia in patients with cancer and could improve their quality of life, but ESA-related safety concerns exist. To evaluate the overall risk of venous thromboembolism (VTE) associated with the use of ESAs, a systematic review and meta-analysis of published randomized controlled trials (RCTs) was performed. The databases of PubMed and Web of Science and the abstracts presented at the American Society of Clinical Oncology conferences were searched to identify relevant clinical trials. Summary incidence rates, relative risks (RRs), and 95% confidence intervals (CIs) were calculated. A total of 12,115 patients with a variety of cancer types from 51 RCTs were identified and included in the meta-analysis. Among patients receiving ESAs, the summary incidence of all-grade VTE was 7.78%. Patients with cancer who received ESAs had increased VTE risks (484 events among 6,301 patients treated with ESA vs. 276 events among 5,814 control patients; RR = 1.75 [95% CI, 1.50–2.05]). The highest risk of VTE was found in patients with ovarian and cervical cancers (RR = 2.45 [CI = 1.12–5.33]). The VTE risk among hematologic malignancies was higher than that among solid tumors. The administration of ESAs was significantly associated with an increased risk of developing VTE in cancer patients receiving these drugs. The risks of VTE may vary with various tumor types, including hematologic malignancies.