After operating as a hotel for almost two decades, the Cottages were purchased by the Cooke family in 1893. Three adult brothers: a doctor, a lawyer and a constable, each owned one section and used it as a family home. The doctor's daughter, Lucy Cooke, familiar to many Cooperstown residents as a piano teacher, lived here until her death in 1974. She had the third section of the building torn down in 1958 to satisfy her desire for a two-car garage. (That garage has since been converted to an apartment.) After Lucy's death, the building passed out of family ownership and was used for offices and apartments.

Michael Jerome, the innkeeper, purchased the deteriorating structure in February 1985. A native of Elmira, Mr. Jerome came to this area specifically seeking a suitable historic structure to run as a hotel.

The Inn at Cooperstown opened in May 1985 after an extensive restoration. The Inn was placed on the National Register of Historic Places and received the New York State Historic Preservation Certificate of Achievement. In 1992, the Preservation League of New York presented their prestigious Tourism Award to The Inn at Cooperstown. The hospitality, service and high standards at The Inn have been recognized with several other awards including Certificates of Distinction in the RIT/USA Today Quality Cup Competitions.

In 1999, Michael Jerome and his wife Marianne Bez, co-owners of The Inn were honored with acceptance into the most prestigious innkeeping organization, the Select Registry of Distinguished Inns of North America. The Inn is one of almost 400 outstanding inns in the United States and Canada included in the Association's lavish guide book.

Since 1985, The Inn has welcomed over 100,000 visitors from around the world. The Inn has been featured in major travel publications including articles in The New York Times, New York Magazine, Travel and Leisure, Adventure Road, Travel Holiday, Conde-Nast Traveler, USA Today and the Los Angeles Times.