The route goes north as Rossville Boulevard, going through suburbs and passing by several businesses before entering Chattanooga and coming to an interchange with Interstate 24 (I-24; exits 180A–B) and briefly running concurrently with the Interstate, having interchanges with SR 58 (Market Street) and US 11/US 41/US 64/US 72/SR 2, before splitting off as a freeway (exit 178).

US 27/SR 29 then narrow to six lanes and runs on top of a ridge while passing through Red Bank, where it has interchanges with Morrison Springs Road (where it narrows to four lanes), Mountain Creek Road, SR 153 southbound, and Dayton Pike northbound (once again, the old route of US 27), before entering Soddy-Daisy.

US 27/SR 61 then pass through Cardiff, where they intersect with the short SR 382, which provides access to Roane State Community College.

They then enter the South Harriman neighborhood and pass by several businesses and rejoin with SR 29 (Ruritain Road).

They then cross the bridge over the Emory River to enter and pass through the historic downtown, intersecting with SR 328.

Just beyond Harriman, near the DeArmond community, US 27/SR 29 then splits from SR 61 at an interchange, with the Harvey H. Hannah Memorial Highway following that route to the east.

In Morgan County, the highway passes through the rugged mountains of the Cumberland Plateau and has another intersection with SR 328 before ascending a ridge to enter Mossy Grove.

It passes through Mossy Grove and has an intersection with Clayton Howard Road, which provides access to Lone Mountain State Forest.

It then leaves the town and continues north to an intersection with Main Street (Old US 27 in downtown) just before entering Wartburg.

US 27/SR 29 then passes through the community of Glenmary before entering Elgin, where the highway intersects SR 52, which connects the area with the historic village of Rugby and Fentress County to the west.

SR 297 then splits off to the west in the center of town, which provides access to the Big South Fork National River and Recreation Area.

[2] The first part of the controlled-access segment, located between Martin Luther King Jr. Boulevard and what is now the interchange with Dayton Pike was built between 1955 and 1959 by moving dirt from nearby Cameron Hill.

[citation needed] The entire route has been widened to a four-lane highway all the way to the second junction with SR 328 near Oakdale.

[7] Beginning in the middle of 2012, the Tennessee Department of Transportation (TDOT) began rebuilding US 27 from the Olgiati Bridge to the interchange with US 127.

[12] The project will widen the route from the existing two to three lanes each direction to three or four lanes each direction (including two more across the Olgiati), straighten out curvy sections, rework the Fourth Street and Martin Luther King interchanges, and add retaining walls.