Cyanobacterial harmful algal blooms (CyanoHABs) are enhanced by anthropogenic pressures, including excessive nutrient (nitrogen, N, and phosphorus, P) inputs and a warming climate. Severe eutrophication in aquatic systems is often manifested as non-N2-fixing CyanoHABs (e.g., Microcystis spp.), but the biogeochemical relationship between N inputs/dynamics and CyanoHABs needs definition. Community biological ammonium (NH4+) demand (CBAD) relates N dynamics to total microbial productivity and NH4+ deprivation in aquatic systems. A mechanistic conceptual model was constructed by combining nutrient cycling and CBAD observations from a spectrum of lakes to assess N cycling interactions with CyanoHABs. Model predictions were supported with CBAD data from a Microcystis bloom in Maumee Bay, Lake Erie, during summer 2015. Nitrogen compounds are transformed to reduced, more bioavailable forms (e.g., NH4+ and urea) favored by CyanoHABs. During blooms, algal biomass increases faster than internal NH4+ regeneration rates, causing high CBAD values. High turnover rates from cell death and remineralization of labile organic matter consume oxygen and enhance denitrification. These processes drive eutrophic systems to NH4+ limitation or colimitation under warm, shallow conditions and support the need for dual nutrient (N and P) control.