Enterocytes present a continuous array of uniform, tightly packed, apical microvilli known as the brush border. Adjacent microvilli tips are linked by an intermicrovillar adhesion complex (IMAC) composed of cadherins that are required for microvillar packing, length uniformity, and junctional integrity, with disruption linked to intestinal autoimmune disease and infections. We found that IMAC-deficient mice have increased adherent (actin-dependent) and mucosal (actin-independent) bacteria in the terminal ileum. These bacteria are primarily commensals without differences in diversity between groups. Initial segments of Segmented filamentous bacteria (SFB) recruit microvilli proteins (EPS8/IRTKS) and Arp2/3 to remodel actin. SFB anchor contiguous to cell junctions and incorporate ZO-1 into their attachments. Together, these data reveal maturation of the SFB host-microbe interface that mirrors the complex SFB lifecycle. Our work indicates a previously unrecognized role for the brush border as a key component of host defense against luminal microbes.