The highway runs 42.822 miles (68.915 km) from MT 41 in Twin Bridges east to U.S. Route 287 (US 287) in Ennis.

The course of MT 287 follows the ultimate portions of two trails that met in Virginia City, the center of the Alder Gulch gold rush of the mid-1860s and the second territorial capital of Montana.

The highway extended north of Twin Bridges to Whitehall until the late 1970s, when it achieved its current length.

Rossiter Building, Christ Episcopal Church and Rectory, and the William O'Brien House.

[2] In Alder, MT 287 leaves the valley of the Ruby River and heads east through Alder Gulch, a narrow valley along which the highway ascends the more moderate mountains between the Tobacco Root Mountains to the north and the Gravelly Range to the south.

MT 287 follows the Alder Gulch Short Line Railroad, an isolated narrow-gauge railway, until the route reaches Virginia City.

MT 287 meets the northern end of S-249 (Varney Road) where the highway curves north on arriving at the Madison River.

[9] The Virginia City–Ennis road was added to the federal aid highway system and designated State Route No.

[10] The highway from Twin Bridges to Virginia City remained an unimproved dirt road.

[1] The reconstructed highway was removed from Middle Road and Tuke Lane to its present course between the two towns.

[1] The reconstructed highway bypassed Bivens Creek Road and for the first time served Laurin directly.

[16][17] Two years later, MT 34 was placed on its modern alignment south through Alder and east through the dredge tailings.

[18][19] MT 34 was reconstructed on or very close to the old road through Alder Gulch to the east end of Virginia City in 1945.

[1][21] Finally, the modern highway from Twin Bridges to Ennis was completed when the route from Virginia City to the summit was reconstructed and paved in 1956.

MT 287 continued with US 10N north and west to Helena, then the route ran concurrently with US 91 (along the modern I-15 corridor) to Wolf Creek.