Voltage gated sodium channels (VGSCs) are required for action potential initiation and propagation in mammalian neurons. As with other ion channel families, VGSC density varies between neurons. Importantly, sodium current (INa) density variability is reduced in pyramidal neurons ofScn1bnull mice. Scn1bencodes the VGSC β1/ β1B subunits, which regulate channel expression, trafficking, and voltage dependent properties. Here, we investigate how variableINadensity in cortical layer 6 and subicular pyramidal neurons affects spike patterning and network synchronization. Constitutive or inducibleScn1bdeletion enhances spike timing correlations between pyramidal neurons in response to fluctuating stimuli and impairs spike-triggered average current pattern diversity while preserving spike reliability. InhibitingINawith a low concentration of tetrodotoxin similarly alters patterning without impairing reliability, with modest effects on firing rate. Computational modeling shows that broadINadensity ranges confer a similarly broad spectrum of spike patterning in response to fluctuating synaptic conductances. Network coupling of neurons with highINadensity variability displaces the coupling requirements for synchronization and broadens the dynamic range of activity when varying synaptic strength and network topology. Our results show thatINaheterogeneity between neurons potently regulates spike pattern diversity and network synchronization, expanding VGSC roles in the nervous system.