Excess ingestion of energy-dense fats promote obesity, metabolic syndrome and insulin-resistant type-2 diabetes, a worldwide public health crisis. In rat models, a high-fat diet (HFD) fed from weaning severely impairs hippocampal function, critical for memory consolidation. Sex differences are rarely systematically assessed in such models. Littermate male and female Long-Evans rats were fed from weaning a control or a HFD (57.6% fat, 26.8% carbohydrate, 15.6% protein) for 12 wk. Spatial memory was assessed in spatial objection recognition (SOR) and spontaneous alternation (SAT) tasks. Rats were then deeply anesthetized with 1% isoflurane, and plasma was collected for ELISAs; estrus was assessed by vaginal cytology; and brain slices rapidly prepared. In vitro recordings were made from CA1 pyramidal neurons to assess post-burst AHPs and accommodation, then plasticity induced by bath applied 12.5 nM insulin. Both sexes consuming HFD showed significantly impaired spatial memory compared to controls. HFD males developed clinically-relevant symptoms of type-2 diabetes (weight gain, loss of blood glucose control, elevated circulating insulin, loss of insulin-sensitivity of CA1 neurons), but HFD females did not (normal body weight, normal blood glucose control, reduced circulating insulin, enhanced insulin-sensitivity of CA1 neurons, with no changes in estrogen nor in estrus). While both males and females exhibited significant deficits on both memory tasks, cognitive deficits in males—presenting with diabetic symptoms—would be easier assess and treat (with strategies appropriate for insulin-resistant diabetes). Females deficits would be covert (no clinical symptoms) and thus likely remain undiagnosed. Given the profoundly different biological responses shown by females to HFD, their cognitive deficits are unlikely to respond to treatments effective in males. These previously undescribed findings suggest different public health issues for females than for males. Consistent with other findings linking intrinsic excitability to memory, HFD enhanced post-burst AHPs and accommodation in both sexes, i.e. reduced intrinsic excitability. CA1 insulin-sensitivity was lost sex-dependently, only in males, consistent with dysfunctional peripheral glucose regulation and increased circulating insulin, symptoms of insulin-resistant type-2 diabetes. Females maintained glucose control, while circulating insulin decreased, and remained insulin-sensitive both peripherally and centrally, previously undocumented effects. These findings illustrate that while cognitive impairments in females are clinically asymptomatic, diagnostic and treatment strategies for the effects of HFDs on males and females should not be the same.