Actin cytoskeleton is a dynamic framework of cytoplasmic filaments that rearranges as the needs of the cell change during growth and development. Incessant turnover mechanisms allow these networks to be rapidly redeployed in defense of host cytoplasm against microbial invaders. However, the precise functions of host actin and the molecular mechanisms underlying actin rearrangements in host defense remain largely unknown. Here, we uncover the mechanism by which host actin controls innate immunity gates on plant surface to actively prevent microbial entry into internal tissue. VLN3, a villin protein from Arabidopsis is a key regulator of this process. Our in vitro and in vivo phosphorylation assays show that VLN3 is a physiological substrate of two pathogen-responsive mitogen-activated protein kinases (MAPKs). Quantitative analyses of actin dynamics and genetic studies reveal that phosphorylation of VLN3 by MAPKs govern actin remodeling to activate innate immunity gating on host surface.