A suite of molecular sensory systems enablesCaulobacterto control growth, development, and reproduction in response to levels of essential elements. The bacterial enhancer binding protein (bEBP) NtrC, and its cognate sensor histidine kinase NtrB, are key regulators of nitrogen assimilation in many bacteria, but their roles inCaulobactermetabolism and development are not well defined. Notably,CaulobacterNtrC is an unconventional bEBP that lacks the σ54-interacting loop commonly known as the GAFTGA motif. Here we show that deletion ofC. crescentus ntrCslows cell growth in complex medium, and thatntrBandntrCare essential when ammonium is the sole nitrogen source due to their requirement for glutamine synthetase (glnA) expression. Random transposition of a conserved IS3-family mobile genetic element frequently rescued the growth defect ofntrCmutant strains by restoring transcription of theglnBAoperon, revealing a possible role for IS3 transposition in shaping the evolution ofCaulobacterpopulations during nutrient limitation. We further identified dozens of direct NtrC binding sites on theC. crescentuschromosome, with a large fraction located near genes involved in polysaccharide biosynthesis. The majority of binding sites align with those of the essential nucleoid associated protein, GapR, or the cell cycle regulator, MucR1. NtrC is therefore predicted to directly impact the regulation of cell cycle and cell development. Indeed, loss of NtrC function led to elongated polar stalks and elevated synthesis of cell envelope polysaccharides. This study establishes regulatory connections between NtrC, nitrogen metabolism, polar morphogenesis, and envelope polysaccharide synthesis inCaulobacter.