Most of the highway was taken over by the state of New York in the 1910s and 1920s. In 1908, the section of modern NY 250 in Fairport between Church and High Streets became part of Route 20, an unsigned legislative route assigned by the New York State Legislature. The definition of the route was altered in 1921, taking the route on a more southerly course that used the portion of what is now NY 250 between NY 31 and NY 31F instead through eastern Monroe County. NY 250 was assigned to its current alignment as part of the 1930 renumbering of state highways in New York.