Food-borne disease due to intestinal parasites (IPs) and enteric bacterial infections (EBIs) remain a major public health problem. Food handlers, individuals involved in preparing and serving food, working with poor personal hygiene could pose a potential threat of spreading IPs and EBIs to the public. The aim of this study was to examine the overall prevalence and risk factors of IPs and EBIs among food handlers in four selected regions of Ethiopia. Scientific articles written in English were recovered from PubMed, ScienceDirect, Web of Science, Google Scholar, Cochrane Library, and other sources from Google Engine and University Library Databases. “Prevalence,” “Intestinal Parasites,” “Enteric Bacterial Infections,” “Associated Factors,” “Food Handlers,” and “Ethiopia” were the search terms used for this study. For critical appraisal, PRISMA 2009 was applied. Stata software version 16 was used to perform the meta-analysis. Heterogeneity and publication bias were evaluated using Cochran's Q, inverse variance (I2), and funnel plot asymmetry tests. A random-effects model was used to calculate the pooled burden of IPs and EBIs and its associated factors among food handlers, along with the parallel odds ratio (OR) and 95% confidence interval (CI). For this meta-analysis, a total of 5844 food handlers were included in the 20 eligible studies. The overall pooled prevalence of IPs and EBIs among food handlers in four selected regions of Ethiopia was 29.16% (95% CI: 22.61, 35.71), with covering (25.77%) and (3.39%) by IPs and EBIs, respectively. Ascaris lumbricoides, Entamoeba histolytica/dispar, Giardia lamblia, and hookworm were the most prevalent IPs among food handlers with a pooled prevalence of 7.58%, 6.78%, 3.67%, and 2.70%, respectively. Salmonella and Shigella spp. were the most prevalent EBIs among food handlers with a pooled prevalence of 2.78% and 0.61%, respectively. A high prevalence of IPs and EBIs among food handlers was observed in Oromia (38.56%; 95% CI: 29.98, 47.14), while a low prevalence was observed in the Tigray region (19.45%; 95% CI: 6.08, 32.82). Food handlers who had not taken food hygiene training (OR: 0.68, 95% CI: −0.34, 1.69), untrimmed finger nail (OR: 2.23, 95% CI: 1.47, 2.99), lack of periodic medical checkup (OR: 1.52, 95% CI: 0.41, 2.64), lack of handwashing habits (OR: 1.97, 95% CI: 0.53, 3.41), and eating raw vegetables and meat (OR: 2.63, 95% CI: 0.92, 4.34) were factors significantly associated with the prevalence of IPs and EBIs. The prevalence of IPs and EBIs was high in the selected Ethiopian region (Amhara, Oromia, SNNPR, and Tigray) food handlers along an increasing prevalence trend from 2014 to 2022. Therefore, this study recommends the provision of proper health education and training regarding personal hygiene, hand washing, food handling, medical checks, as well as raw vegetable and meat safety.