The western terminus of the route was at an intersection with NY 36 in the hamlet of Mumford within the town of Wheatland.

NY 35 followed a mostly northeast–southwest routing across the counties of Monroe and Wayne and passed through downtown Rochester.

Instead of turning west onto Elmwood Avenue at then-NY 47, NY 35 veered north onto Genesee Street.

After crossing the river, the two routes met US 15 at its northern terminus at Clinton Avenue.

There, it passed through the southern portion of Ellison Park and crossed Irondequoit Creek before turning sharply to the northeast to meet the eastern terminus of NY 35B.

Also created in 1908 was Route 15, which initially began in Hornell and ended in Caledonia.

[3] In the 1930 renumbering of state highways in New York, NY 35 was extended northeastward to the hamlet of Ontario Center by way of downtown Rochester.

[12][13] NY 35 was truncated and slightly rerouted c. 1938 after US 20 was moved onto its current alignment through Western New York.

The remainder of the route in Walworth and Ontario became an extension of NY 350, which had previously ended at a junction with then-NY 33B north of Macedon.