Zoonotic parasites, including Toxocara species, of pet and stray cats are of public health importance. Justification for, and the design and implementation of prevention and control of human toxocariasis may benefit from an understanding of the zoonotic potential and prevalence of parasites in this definitive host species. This is the first systematic review and meta-analysis of cross-sectional studies, conducted to estimate the prevalence of Toxocara infection(s) in cats by geographical location, type (rural vs urban and stray vs pet), gender and age. Pooled data were assessed using a random effects-model as well as several meta-regression and stratified analyses conducted. Of 1733 peer-reviewed articles, 143 were included in this review and represented 2,158,069 cats from 51 countries. The global pooled (95% CI) prevalence of Toxocara infection in cats was 17.0% (16.1–17.8%), being highest in African (43.3%, 28.3–58.4%) and lowest in South American (12.6%, 8.2–17.0%) countries. In other WHO regions, prevalence rates of Toxocara were as follows: Eastern Mediterranean (21.6%, 15.1–28.1%), North America (18.3%, 15.4–21.2%), Europe (17.8%, 15.9–19.7%), Western Pacific (17.3%, 14.7–19.9%), and South-East Asia (14.9%, 9.8–20.1%). Prevalence of Toxocara was higher in low-income tropical countries and also in stray (28.6%, 25.1–32.1%) and young (≤ 12 months of age) (27.7%, 23.4–32.0%) cats than in pet (11.6%, 10.7–12.5%) and older cats (> 12 months of age) (23.8%, 14.8–32.7%). This review indicates that ~ 118–150 million cats worldwide serve as definitive hosts of Toxocara, shedding eggs and thus contributing to the public health risk of human infection. Prevention and control of this zoonosis in cats should receive greater attention by health officials and cat owners, particularly in countries where risk factors and prevalence are highest.