Mycobacteria have plagued humanity for all recorded history and helped lay the foundation for modern understanding of infectious disease etiology, yet our understanding of their basic cell biology is only just emerging. The composition and structure of mycobacterial cell envelopes are particularly unique among well studied bacteria, as are the mechanisms by which they elongate and divide. Mycobacteria accumulate two mycobacterial lipoglycans lipomannan (LM) and lipoarabinomannan (LAM) in their cell envelopes, though their functions have remained unclear. In the model mycobacterial species Mycobacterium smegmatis, we show that the size and presence of LAM plays a nutrient-dependent role in modulating cell wall integrity at sites of division. Using an attenuated Mycobacterium tuberculosis strain, we also demonstrate that these phenotypes are conserved in pathogenic mycobacteria. Furthermore, we go on to identify phosphate and certain amino acids as two key nutritional components that reduce the fitness of LAM-deficient mycobacteria, and we propose a potential molecular mechanism based on changes in gene essentiality in a LAM mutant.