The section of highway between its southern terminus near Winnipeg and the second junction with PTH 68 near Eriksdale is part of the Northern Woods and Water Route.

It heads west, concurrent (overlapped) with the Northern Woods and Water Route, to meet PR 236 at a Roundabout and cross the Prairie Dog Central Railway, where it curves northwest and begins paralleling the rail line as it goes through a switchback.

The highway curves due northward at the community of Oak Point, leaving the lake's coastline and crossing into the Rural Municipality of Coldwell.

The now enters the Rural Municipality of West Interlake and almost immediately passes through Deerhorn, where it curves due northwest again and to mostly bypass the town of Ericksdale within the next few kilometers, having an intersection with PR 417 and becoming concurrent with PTH 68 here.

It travels through the community of Hilbre as it comes within 3 kilometres (1.9 mi) of the southern shores of Lake St. Martin.

PTH 6 temporarily leaves the Rural Municipality of Grahamdale, traveling through the Pinaymootang First Nation and crossing the Fairford River at the Fairford River Water Control Structure (FRWCS / a dam), just a little 1 kilometre (0.62 mi) from its mouth on the northeast shore of Lake Manitoba.

The highway re-enters the Rural Municipality of Grahamdale and leaves the proximity of Lake Manitoba for good, traveling past Lake Pineimuta and through the community of St. Martin Junction, where and it has an intersection with PR 513, before having junctions with PR 328 and Road 190 North (provides a second access road to Gypsumville).

PTH 6 crosses the northern part of town, having intersections with Grand Rapids Drive / Campbell Avenue (the town's Main Street) and Government Road (provides access to the dam and Hybord) before leaving Grand Rapids and the vicinity of Lake Winnipeg to cross into Division No.

[11] In 1928, PTH 6 was originally designated to travel from Minnedosa to the Saskatchewan border southwest of Benito via Dauphin and Swan River.

It passes through a neighbourhood before joining PTH 6 in a concurrency (overlap), following it for a couple kilometres as the two bypass downtown along its western side.

PR 237 splits off and heads due east, leaving Moosehorn travelling through wooded areas for 5.5 kilometres (3.4 mi) before making a sharp left to enter Spearhill, where the PR 237 designation ends and the road continues north as Spearhill Road.

The highway winds its way southeast as it passes by a reservoir and a quarry before heading due eastward through rural areas for the next several kilometres.

Provincial Road 375 (PR 375) is a short 4-kilometre-long (2.5 mi) east-west spur of PTH 6 in the Local Government District of Mystery Lake.

It is entirely a two-lane gravel road, traversing the southern coastline of Lake Francis for around half its length.

Provincial Road 417 (PR 417) is a 24.8-kilometre-long (15.4 mi) east-west spur of PTH 6 in the Rural Municipality of West Interlake, running westward from its intersection with PTH 68 in Eriksdale to the Lake Manitoba First Nation on the shores of southern Lake Manitoba, having a junction with PR 418 along the way.

Provincial Road 513 (PR 513) is a 50.7-kilometre-long (31.5 mi) east-west spur of PTH 6 in the Rural Municipality of Grahamdale and Unorganized Division No.

PR 513 makes a sharp turn to the north and begins following the left bank of the Dauphin River, meandering through the remote woodlands of Unorganized Division No.