Phyllosphere microbiota is thought to play a critical ecosystem function on earth. However, little is known about the molecular mechanism underlying how plants maintain phyllospere microbiota homeostasis for health. Here we characterized an Arabidopsis mutant, ben3, described previously to carry a mutation in an ARF-GEF gene, BIG2. However, we found that the ben3 mutant exhibited hypersusceptibility to endogenous phyllosphere microbiota, but an independent big2 mutant did not. Interestingly, ben3 mutant displayed poor phyllosphere health in a microbiota-dependent manner toward the inoculation of SynComCol-o, a synthetic phyllosphere microbiota from Arabidopsis Col-0. Bulk segregation and next-gen sequencing of the ben3 mutant revealed that microbiota hypersusceptibility is caused by a second mutation in a gene which we called Guardian of Normal Microbiota 1 (GRM1). We have shown that elicitors of pattern-triggered immunity can induce the expression of the GRM1 protein. In addition, when grown in conventional soil (i.e., in the presence of natural microbiota), the ben3 mutant showed spontaneously activated expression of defense genes. Illumina Miseq sequencing of using 16S rRNA gene is underway to reveal possible shifts in the endophytic bacterial composition in the ben3 phyllosphere. Altogether, our results indicated that the GRM1 gene is a strong candidate for playing a major role in controlling microbiota homeostasis in the Arabiodpsis phyllopshere.