The Ministry of Transportation of Ontario was once responsible for the length of the route, when it ran from Long Branch to Highway 93 in Waverley.

Today, only the southernmost 1.6 km (1 mi) from Highway 427 north to Mimico Creek is under provincial jurisdiction, the remainder of the route is maintained by the city of Toronto, York Region and Simcoe County.

South of Kleinburg, the highway dipped into the Humber River valley, connecting with Islington Avenue.

Continuing north again, the highway meandered towards Georgian Bay, departing from the old Penetanguishene Road at Mertz's Corner.

The route curved around the western side of a large marsh before entering the community of Wyebridge, where it crossed the Wye River.

It was completed and opened to traffic in 1938, bringing Highway 27 to its peak length of 148.1 km (92.0 mi).

The junction with the QEW was built over 48.5 ha (120 acres) and required the construction of 19 bridges and the equivalent of 42 km (26 mi) of two lane roadway.

[10] The junction with Highway 401 sprawls over 156 ha (385 acres) and required the construction of 28 bridges and the equivalent of 46.6 km (29 mi) of two lane roadway, the largest interchange in Canada.

Originally, northbound traffic had to turn east at Highway 9 then north at Leonard Road; a smooth curve is visible at this latter intersection, though it now forms the driveways of several residences.

[20] Within the City of Toronto it is locally maintained, and still known as Highway 27; a proposal to rename it to "Etobicoke Drive" was rejected.

[7] The following table lists the major junctions along Highway 27, as noted by the Ministry of Transportation of Ontario.