Understanding pathogen emergence in new host species is fundamental for developing prevention and response plans for human and animal health. We leveraged a large-scale surveillance dataset coordinated by United States Department of Agriculture, Animal and Plant Health Inspection Service and state natural resources agencies to quantify infection of SARS-CoV-2 in North American white-tailed deer (Odocoileus virginianus; WTD) using a hierarchical epidemiological model in the eastern half of the United States. Our model found that male deer had higher positivity than female deer, and positivity was higher in counties with higher human population density or deer habitat. Estimated SARS-CoV-2 local epidemiological reproduction numbers were between 1 and 2.5 in most well-sampled counties, with local epidemics in WTD peaking earlier in the northeast and mid-Atlantic relative to the Midwest and Southeast. Similar peak infection prevalence times across many counties provided indirect evidence for widespread transmission via human-to-deer spillover, while the widespread high estimates of local epidemiological reproduction number suggested that sustained deer-to-deer transmission is also probable. The model estimated 10% of infected WTD were infected due to human infection pressure.