[1][2] The museum's mission is to connect its audience to American and New York State cultural heritage by organizing exhibits and public programs that "engage, delight and inspire.

In 1939, Stephen Carlton Clark, an art collector interested in history, who also served on the board of the Museum of Modern Art and the Metropolitan Museum, invited NYSHA to move to Fenimore House, the mansion of his late brother Edward Severin Clark on land that was part of James Fenimore Cooper's former farm just outside Cooperstown.

[3] Having operated under a dba as Fenimore Art Museum since the 1990s, and in an effort to better describe its wide-ranging activities, the organization applied to amend its charter and change its corporate name in 2017.

[13] In 1968, a separate building was built to consolidate the library collections of both New York State Historical Association (as it was known at the time) and The Farmers' Museum.

[2] Since 2015 the museum has hosted outdoor theatrical productions in the Lucy B. Hamilton Amphitheater, located on the grounds overlooking Otsego Lake.