The highway also serves as the primary route from Toronto to southern Georgian Bay and Muskoka, areas collectively known as cottage country.

Since the 1970s to the present there have been numerous projects which have widened and modernized the freeway between North York and Barrie, including being expanded with a collector-express system in Vaughan to accommodate the interchange with the new Highway 407 ETR.

[2] South of that, the route continues as the municipal Black Creek Drive, an arterial road or limited controlled-access expressway with at-grade intersections, originally planned as a southern extension of Highway 400.

North of Langstaff Road, the freeway passes west of Vaughan Mills shopping centre and Canada's Wonderland theme park.

[10] The highway passes through protected rural areas in northern York Region and encounters rolling countryside in Simcoe County south of Barrie.

[16][17] At Port Severn, the highway meets the rugged Canadian Shield, and winds its way north through the granite, often flanked by towering slabs of rock.

[3] The onset of the Korean War slowed construction on the highway considerably,[18] and it wasn't until December 1, 1951 that two lanes (one in each direction) would be opened to traffic.

The torrential downpours caused catastrophic damage to southern Ontario, amongst which was the flooding of Holland Marsh to a depth of 3.3 m (11 ft).

[23] For many years afterwards, and still today to older drivers, this portion of the highway (or sometimes even the entire stretch to Parry Sound) north of Barrie is referred to as the "400 Extension".

[26] Highway 400 would still open as far south as Jane Street on October 28, 1966,[27] before the rest of the plans were shelved following the cancellation of the Spadina Expressway.

[28] The province used the right-of-way in the Black Creek valley to construct a four-lane divided expressway with signalized intersections as far south as Eglinton Avenue, although there was sufficient space for a six-lane freeway with interchanges.

Originally known as the Northwest Arterial Road, the expressway opened in 1982 as Black Creek Drive and was transferred to Metropolitan Toronto on March 1, 1983.

In exchange, the City of Toronto was given expropriated land purchased for Spadina south of Eglinton Avenue in order to block a further southward extension of Allen Road.

In 1988 construction began on the southbound structures over Matchedash Bay and the Canadian National Railway crossing north of Highway 12.

In 1988 construction began on the southbound structures over Matchedash Bay and the Canadian National Railway crossing north of Highway 12.

[16][40] However, a land claim dispute between the Government of Ontario and the Wahta Mohawks prevented the twinning of the highway between the Musquash and Moon Rivers.

The Territorial Reserve did not oppose the construction; however, the land was unobtainable due to a technicality requiring a minimum voter turnout of 65 percent.

[41] Construction of the Parry Sound Bypass, a new alignment from Badger Road to the Seguin River, began with an interchange along Highway 518 at the site of the future freeway, which was completed during the autumn of 1999.

[46] This was followed a year later on October 7 with the opening of the bypass of Highway 69 from the Moon River to Rankin Lake Road, connecting with the Parry Sound segment.

[2] As one of the oldest 400-series freeways, several vintage overpasses have been demolished in recent years to accommodate the future widening of Highway 400 to ten lanes in the section from Vaughan to Barrie.

Sixteen of these historic structures, sub-standard by today's freeway requirements, remained as of summer 2009, with all slated for replacement in the near future.

In order to preserve some of this heritage the Ministry of Transportation created an 1800mm x 1625mm reusable urethane mould of the provincial coat-of-arms from the 5th Line overpass located south of Bradford, which will be used to decorate the replacement structures.

[52] The Highway 9 (Davis Drive) overpass was initially twinned with an addition span on the north side in the late 1990s,[citation needed] however this still permitted only six lanes of Highway 400 to pass underneath, so a decade later the twin structures were replaced with a wider single bridge that was long enough to accommodate future widening of the freeway to eight lanes.

[56] The new structure which is designed for higher travel speeds, and also long enough to accommodate future expansion of Highway 11 underneath, was completed in October 2015.

[60][61][62] As a precursor to the eventual reconfiguration of the Highway 89 junction, the Cookstown service centre was closed on February 1, 2013, while its replacement was shifted to a new site north of Fourth Line while being rebranded as Innisfil ONRoute and it reopened in June 2015.

[63] Construction to replace the Highway 89 overpass and realign the interchange to a parclo, with new ramps to be built in the NW quadrant where the service centre was formerly located, commenced in 2019 with an expected completion set for 2021.

The former route of Highway 69 through the town was renamed as Nobel Drive and was reduced in width from four to two lanes, with a recreational trail constructed alongside the road.

In response, the MTO put the operation of the full network of service centres out for tender, resulting in a 50-year lease with Host Kilmer Service Centres, a joint venture between hospitality company HMSHost (a subsidiary of Autogrill) and Larry Tanenbaum's investment company Kilmer van Nostrand, which operates them under the ONroute brand.

[75] Three of the four service centres were upgraded and feature a Canadian Tire gas station, an HMSHost-operated convenience store known as "The Market", as well as fast food brands such as Tim Hortons, A&W and Burger King.

The Cookstown centre was located at the Highway 89 interchange being incorporated into the southbound ramp (while accessible to northbound traffic by exiting on westbound Highway 89 then turning at a driveway on the west side of the 400) and it closed on February 1, 2013, while its replacement was shifted to a new site north of Fourth Line while being rebranded as Innisfil ONRoute and it reopened in June 2015.