It is concurrent with U.S. Route 19 (US 19) from exit 4 (Interstate 285) until its northern terminus south-southeast of Dahlonega, linking the city of Atlanta to its north-central suburbs and exurbs.

SR 400 travels from the Lindbergh neighborhood in the Buckhead district of Atlanta, at Interstate 85 (I-85), to just south-southeast of Dahlonega.

Between I-85 and I-285, SR 400 is designated "T. Harvey Mathis Parkway", after a local land developer and road proponent who died the day after being appointed as head of the Atlanta Committee for the Olympic Games in June 1991, when the tollway was under construction.

Upon reaching the Perimeter (I-285) and beyond, the highway is designated "Turner McDonald Parkway", after a Fulton County Public Works Department director.

SR 400's exit 6 at Northridge Road is known as the Mayor Eva Cohn Galambos Memorial Interchange.

SR 400 continues into Lumpkin County just south of its intersection with Whelchel Road and Wilson Drive.

SR 400 ends at this point, and US 19 turns left and continues north through downtown Dahlonega into the Appalachian Mountains and the Chattahoochee–Oconee National Forest.

On I-85 south, drivers had to take the Cheshire Bride Road/Lenox Road exit to get to Sidney Marcus Boulevard for access onto SR 400 north.

In January 1974, the Georgia General Assembly named a stretch of the highway — from I-285 to the Fulton-Forsyth county line — after McDonald.

In 2005 the GDOT began widening the section from Holcomb Bridge Road to McFarland Parkway from six to eight lanes.

The northern portion of the inside-the-Perimeter route remained alive following the freeway revolts, and after lawsuits by residents that spent several years in court, GDOT was able to force the extension through Buckhead.

Dozens of homes were taken through eminent domain or the threat of it, and the highway was built through the middle of formerly-secluded and forested neighborhoods.

A compromise was worked out for Fulton County to pay $3 million to Robinson-Humphrey to offset extra construction costs.

[13] Atlanta City Council member Buddy Fowlkes was opposed to the extension of GA 400; "I'm encouraged," he said in 1989.

[16] Existing exits were renumbered up by four to accommodate the extension[citation needed], which had a single toll plaza in the middle of its length when opened.

In June 2015, a ceremony was held to name the flyover bridges for Captain Herb Emory, a beloved local traffic reporter for WSB AM and WSB-TV (as well as other co-owned stations) who had died in April 2014.

The point where this road would have had its interchange with the also-doomed I-485 (now Freedom Parkway and SR 10 to Stone Mountain Freeway) is now the site of the Jimmy Carter Library and Museum.

A later routing of I-485 would have had that number running from the Downtown Connector east to the current library, then north on what is now SR 400.

As of September 2024, the project is not on the GDOT's Major Mobility Investment Program List[18] Funding for a project to create a new interchange on SR 400 at SR 369/Browns Bridge Rd came from the Forsyth County Transportation Bond, approved by voters in 2014, along with GDOT funding.

On September 24, 2010, then Governor Sonny Perdue and members of the State Road and Tollway Authority (SRTA) voted to keep the tolls on until 2020 in order to fund 11 new projects on the highway.

[28] In 2012, a feasibility study was initiated by the Georgia Department of Transportation to explore the possibility of adding tolled express lanes.

[36] The project is expected to cost $800 million and is estimated to save drivers on SR 400 and I-285 a combined 20,000 hours of driving time each day.

[37] The project will also include:[34][35][36] Construction was originally expected to be completed by 2020, but due to discovering unmarked utility lines, and labor shortages & supply-chain problems as a result of the COVID-19 pandemic, will now continue into 2025.

[42] In addition, a bus rapid transit system, Georgia's first, will run along the express lanes; the system will possibly include bus access to stops at or near the North Spring MARTA station, Holcomb Bridge Rd, North Point Mall, Old Milton Pkwy, and an existing MARTA park and ride at Windward Pkwy.

[40] Construction was to begin in 2021, but due to increased costs (which exceeded GDOT's $1.7 billion budget) had to be delayed.

[43] A new developer is expected to be announced in early 2024, construction to begin in 2025, and substantial completion to take place in 2031.

[45] GDOT is also working on environmental studies for express lanes along the top end of I-285, from Paces Ferry Rd to Henderson Rd, with construction slated to start in 2023 and finish in 2029.