Originally named Aurora House, the Aurora Inn was built in 1833 by
Colonel E. B. Morgan, a native of Aurora and original investor in The New York Times. By the mid-19th century, Aurora became a major stop on the Erie Canal for boats carrying agricultural products from area farmers to New York City. Henry Wells, of Wells Fargo stagecoach fame and the founder of American Express, established Wells College there in 1868.

During its colorful past, the Aurora Inn was a favored overnight destination for travelers borne by coach, canal boat and rail. It has long been a popular gathering spot for students from Wells, Cornell University and other nearby colleges.

In the early 1840s, William D. Eagles purchased the inn and engaged his uncle John Eagles, a former sea captain, to manage it for him.

When a fire destroyed the main building at Wells College in 1888, many students lived temporarily at the Aurora Inn, which they renamed the Wayside Inn. Fire struck again on February 18, 1919, destroying Aurora’s tiny business district between the old post office and the Aurora Inn. When the south cornices of the inn caught fire, Wells College President Kerr Duncan McMillan climbed onto the roof and helped to douse the blaze.

In 1943, the inn was deeded to Wells College. Despite a series of additions, renovations and new managers, the inn struggled financially starting in the 1970s. A drain on the college's resources, the inn had to be closed several times during the last three decades, most recently in October 2000.

The Aurora Foundation, a partnership between Wells College and the Pleasant T. Rowland Foundation, began a complete renovation of the inn in 2001 to restore its lost luster and make it appealing once again for lodging, dining and special events. The inn reopened in May 2003 to rave reviews by visitors and media alike. It now stands as the crown jewel in the revitalization of Aurora, which is listed on the National Register of Historic Places, along with Wells College and many homes in the village.