The formation of intracellular inclusions containing exon 1 fragments of Huntingtin (Httex1) is a central facet of Huntington Disease pathology.  What remains incompletely understood however is how this process relates to cell damage.  Through a fortuitous discovery with a genetically-encoded biosensor of Httex1 conformation, we found cells formed cytoplasmic inclusions in one of two subtypes we designated PFRi and HFRi. The PFRi subtype comprised Httex1 in an amyloid conformation whereas HFRi contained aggregated Httex1 in a non-amyloid and more disordered conformation. The HFRi were marginally smaller in size to PFRi but otherwise morphologically indistinguishable. The HFRi formed proportionally more frequently with longer pathological polyglutamine lengths; and inversely with expression level.  Cells with HFRi lived significantly longer than cells with PFRi independently of protein expression levels. HFRi had a similar mitochondrial membrane potential to cells without aggregates; whereas cells with PFRi had a severely compromised membrane potential. HFRi death rates occurred almost exclusively via apoptosis whereas those with PFRi died via necrosis. Our data suggests a mechanism by which cells respond to the Httex1 aggregation crisis by diverting into two different physiological states. The PFRi inclusion state is associated with senescence and metabolic shutdown; perhaps caused by untempered amyloid formation of Httex1 damaging core cellular activities.  The HFRi inclusion state is associated with a more functional metabolic state, which may reflect active – and ultimately futile- proteostasis mechanisms to mitigate and remodel the Httex1 into less toxic forms.