Haploid induction is an important tool in crop breeding. Phospholipase A1 (ZmPLA1) / NOT LIKE DAD (NLD)/ MATRILINEAL (MTL) is a key gene controlling haploid induction in maize; however, its molecular mechanism is unknown. To understand the regulatory network of zmpla1, we applied a comprehensive functional analysis at multiple omic levels, integrating transcriptomes, metabolomes, quantitative proteomes and protein modifications. Functional classes of significantly enriched or differentially abundant molecular entities were associated with the oxidative stress response, suggesting that a reactive oxygen species (ROS) burst plays a critical role in haploid induction. In support of this, we show that a simple chemical treatment of pollen with ROS reagents leads to haploid induction (HI). Moreover, a sperm-specific peroxidase (ZmPOD65) was identified as a new gene controlling HI. The mechanism of HI revealed in this study suggests the importance of ROS balance in maintaining normal reproduction, and provides a potential route to accelerate crop breeding.