The cell wall represents an essential structure conserved among most bacteria, playing a crucial role in growth and development. While extensively studied model bacteria have provided insights into cell wall synthesis coordination, the mechanism governing polar growth in actinobacteria remains enigmatic. Here we identify the stomatin-like protein StlP as a pivotal factor for orchestrating polar growth in filamentous actinobacteria under hyperosmotic stress. StlP facilitates the establishment of a membrane microdomain with increased membrane fluidity, a process crucial for maintaining proper growth. The absence of StlP leads to branching of filaments, aberrant cell wall synthesis, thinning of the cell wall, and the extrusion of cell wall-deficient cells at hyphal tips. StlP interacts with key components of the apical glycan synthesis machinery, providing protection to filaments during apical growth. Introduction of StlP in actinobacteria lacking this protein enhances polar growth and resilience under hyperosmotic stress, accompanied by the formation of a membrane microdomain. Our findings imply that stomatin-like proteins, exemplified by StlP, confer a competitive advantage to actinobacteria encountering hyperosmotic stress. Given the widespread conservation of StlP in filamentous actinobacteria, our results propose that the mediation of polar growth through membrane microdomain formation is a conserved phenomenon in these bacteria.