Some previous studies already investigated potential associations between folate metabolism enzyme polymorphisms and lung cancer (LC). However, the results of these studies were inconsistent. Thus, we performed this meta-analysis to explore associations between folate metabolism enzyme polymorphisms and LC in a larger pooled population. Systematic literature research of PubMed, WOS, Embase and CNKI was performed to identify eligible studies. Review Manager Version 5.3.3 was used to conduct statistical analyses. Totally 37 genetic association studies were included for analyses. The pooled analyses showed that MTRR rs1801394 (dominant model: p = 0.01; recessive model: p = 0.04; allele model: p = 0.005) and MTHFR rs1801133 (dominant model: p = 0.008; recessive model: p = 0.0003; allele model: p = 0.0002) polymorphisms were both significantly associated with susceptibility to LC in overall population. Subgroup analyses revealed similar significant findings for MTHFR rs1801133 polymorphism in East Asians. Significant associations with LC were also observed for MTRR rs1801394 and MTHFR rs1801133 polymorphisms in smokers. In conclusion, this meta-analysis indicated that MTRR rs1801394 was significantly associated with LC in smokers, and MTHFR rs1801133 polymorphisms was also significantly associated with LC in smokers and East Asians. These results suggested that these two polymorphisms could be used to identify individuals at high risk of developing LC in certain populations.