Essentials We performed a pooled analysis of 926 patients with cancer‐associated incidental pulmonary embolism (IPE). Vitamin K antagonists (VKA) are associated with a higher risk of major hemorrhage. Recurrence risk is comparable after subsegmental and more proximally localized IPE. Our results support low molecular weight heparins over VKA and similar management of subsegmental IPE. Summary Background Incidental pulmonary embolism (IPE) is defined as pulmonary embolism (PE) diagnosed on computed tomography scanning not performed for suspected PE. IPE has been estimated to occur in 3.1% of all cancer patients and is a growing challenge for clinicians and patients. Nevertheless, knowledge about the treatment and prognosis of cancer‐associated IPE is scarce. We aimed to provide the best available evidence on IPE management. Methods Incidence rates of symptomatic recurrent venous thromboembolism (VTE), major hemorrhage, and mortality during 6‐month follow‐up were pooled using individual patient data from studies identified by a systematic literature search. Subgroup analyses based on cancer stage, thrombus localization, and management were performed. Results In 926 cancer patients with IPE from 11 cohorts, weighted pooled 6‐month risks of recurrent VTE, major hemorrhage and mortality were 5.8% (95% confidence interval CI 3.7–8.3%), 4.7% (95% CI 3.0–6.8%), and 37% (95% CI 28–47%). VTE recurrence risk was comparable under low molecular weight heparins (LMWH) and vitamin K antagonists (VKAs) (6.2% vs. 6.4%; hazard ratio HR 0.9; 95% CI 0.3–3.1), while 12% in untreated patients (HR 2.6; 95% CI 0.91–7.3). Risk of major hemorrhage was higher under VKAs than under LMWH (13% vs. 3.9%; HR 3.9; 95% CI 1.6–10). VTE recurrence risk was comparable in patients with an subsegmental IPE and those with a more proximally localized IPE (HR 1.1; 95% CI 0.50–2.4). Conclusion These results support the current recommendation to anticoagulate cancer‐associated IPE with LMWH and argue against different management of subsegmental IPE.