While the host genetics is known to affect the composition of intestinal microbial communities, whether the host genotype influences the abundance of intestinal commensals remains uninvestigated. To close this knowledge gap, we performed a genome-wide association study (GWAS) in the fruit fly Drosophila melanogaster to identify host genetic variants linked to the abundance of Lactiplantibacillus plantarum – a major gut commensal of fruit flies. Our GWA study uncovered a statistically significant association between polymorphisms in genes involved in heparan sulfate synthesis and L. plantarum load. RNAi-mediated knockdown of some of these genes resulted in reduced heparan sulfate synthesis and reduced abundance of L. plantarum. Thus, heparan sulfate mediates Drosophila gut colonization by L. plantarum. Mechanistically, heparan sulfate facilitates the adhesion of L. plantarum to host epithelium and promotes biofilm formation. We further showed that intestinal infection induces heparan sulfate synthesis by the host via activation of the Nf-kB immune signaling cascade. Increased availability of heparan sulfate during infection results in the expansion of L. plantarum population in the gut. Importantly, such commensal expansion is also beneficial for the host as L. plantarum protects the host from intestinal pathogens via colonization resistance. This work reports an intriguing case where commensal not only survives the inflammatory environment caused by the infection but also benefits from it by utilizing the additional resources made available during infection.