That route was realigned as well in the early 1940s to head southeast from Mount Morris to Dansville, giving way to NY 408.

NY 408, like its predecessor, initially extended southwest from Dalton to Hinsdale in Cattaraugus County via Angelica.

It follows a mostly straight and rural road, save for one easterly deviation to bypass a hill, for 2 miles (3.2 km) to the village of Nunda, where it takes the name State Street.

Midway along this stretch, County Route 3 (CR 3),[4] formerly the westernmost portion of NY 258,[5] leaves to the east.

A slight descent starts a straight route across the low-lying wetlands next to the Genesee River, and I-390 is visible in the distance.

[4] Immediately after crossing Canaseraga Creek, a tributary of the Genesee River, NY 408 meets I-390 at the freeway's exit 7.

[1] Most of what is now NY 408 was originally part of one of several unsigned legislative routes assigned by the New York State Legislature in the early 20th century.

[7] The remainder of modern NY 408 did not become part of a legislative route; however, it was taken over by the state of New York by 1926 nonetheless.

[14][15] The portion of NY 408's former routing between NY 70 and Church Street in Dalton remained state-maintained until April 1, 1983, when ownership and maintenance of the road was transferred to Livingston County as part of a highway maintenance swap between the two levels of government.