NY 40 originally extended south to East Greenbush and north to Comstock when it was assigned as part of the 1930 renumbering of state highways in New York.

At the junction with CR 126, NY 40 turns northward, drops the moniker of Speigletown Road and changes into a much more rural roadway.

Passing some residences as it winds northward, the route meets the junction with CR 122 as it enters the populated hamlet of Grant Hollow.

Bypassing the center of Grant Hollow, NY 40 soon reaches the hamlet of Melrose, where it meets with the junction with CR 117 (Melrose–Valley Falls Road).

After the junction with Casey Road, the route makes a northerly dash to the county line, where it crosses just north of Molesky Lane.

Just after the line, the route enters the hamlet of Crandall Corners, where it junctions with the eastern terminus of CR 54.

Through Barkers Grove, the route passes several local residences and winds north into the hamlet of Easton.

Continuing north through Greenwich, NY 40 turns northeast at a junction with CR 77 (Bald Mountain Road).

NY 40 continues north through the town of Argyle, remaining the two-lane rural roadway it has been through most of the municipality.

North of the hamlet, the route returns to its rural surroundings, reaching a junction with another piece of CR 23.

[3] For a short distance north of CR 23, NY 40 crosses through the town of Fort Ann, based near a junction with Whitney Road.

This junction marks the northern terminus of NY 40, whose right-of-way continues north as Sheehan Road Extension.

[3] NY 40 was assigned as part of the 1930 renumbering of state highways in New York to an alignment extending from East Greenbush in the south to Comstock in the north via the city of Troy and the hamlet of Middle Granville.

The route left its current alignment north of the hamlet of Hartford and headed northeast to Middle Granville, where it met NY 22.

Instead of heading northeast from Hartford, NY 40 went northward to West Granville, where it rejoined its previous alignment.

It now left US 4 in the town of North Greenbush (south of Troy) and followed Winter Street northeastward into the city.

The portion of NY 40's routing between Hartford and West Granville was a sub-par road at the time (deemed as a second and third-class highway by map cartographer General Drafting),[7][8] which led the state to place the end of the route in Hartford instead.

[citation needed] In the late 1950s, NY 40 was cut back on its southern end to begin at what had been the northern terminus of its overlap with US 4 in North Greenbush.

[15] On April 1, 1980, ownership and maintenance of the portion of NY 40 that lies south of NY 142 and outside of the Troy city limits was transferred from the state of New York to Rensselaer County as part of a large highway maintenance swap between the two levels of government.

[19][20] However, the portion of NY 40A's old alignment between the southern Valley Falls village line and NY 67 remained state-maintained until April 1, 1980, when ownership and maintenance of it was transferred to Rensselaer County as part of a large highway maintenance swap between the state and the county.