Epidemiological studies suggest that alcohol use disorder (AUD) is a risk factor for Alzheimer's disease (AD), yet the mechanisms underlying this relationship are poorly understood. Preclinical studies consistently show that chronic, high dose ethanol exposure increases amyloid-β (Aβ) and tau pathology, hallmarks of AD, in rodent models. Conversely, other studies suggest that moderate ethanol consumption may also be protective against AD-related pathology. Thus, we used a modified two-bottle choice paradigm to identify how chronic ethanol exposure, at moderate levels, alters Aβ-related pathology, cognitive performance, and metabolism. Over the course of the experiment, APP/PS1 mice consumed more ethanol than wild-type mice. This led to changes in food and water consumption in APP/PS1 mice, where ethanol-exposed APP/PS1 mice displayed a circadian shift in eating behavior. Ethanol-exposed APP/PS1 mice displayed glucose intolerance, a marker of insulin resistance, even though fasting blood glucose levels and body weights were comparable across all groups. Ethanol-exposed APP/PS1 mice exhibited deficits in nest building, a metric of self-care, as well as increased locomotor activity and central zone exploration in an open field test. Ethanol exposure also led to decreased brain mass, specifically in APP/PS1 mice, suggesting an interaction between ethanol exposure, amyloid pathology, and neurodegeneration. While there was a trend towards increased cortical Aβ deposition, there was a shift in the distribution of plaque size and numbers, with ethanol-exposed APP/PS1 mice showing a greater number of smaller plaques than H2O-exposed APP/PS1 mice. Finally, we used in vivo microdialysis to explore whether acute ethanol modulates hippocampal interstitial fluid (ISF) Aβ and ISF glucose levels in unrestrained, APP/PS1 mice. Acute intraperitoneal injection of ethanol led to a rapid rise in ISF ethanol and directly ISF Aβ (e.g. decreasing during acute exposure and increasing during acute withdrawal), and ISF glucose levels in the hippocampus. Together, these studies indicate that chronic ethanol, even at moderate doses, is sufficient to exacerbate an Alzheimer's-like phenotype in APP/PS1 mice through the direct modulation of Aβ.