SR 40 also serves as the majority of the route from I-95 to Naval Submarine Base Kings Bay and Cumberland Island National Seashore.

[3] SR 40 from Folkston to Kingsland became one of ten stretches of highway designated part of the Okefenokee Trail by the state legislature in 2006.

The road expands to a four-lane divided highway for about 2 miles (3.2 km) before reverting to two lanes shortly before crossing the Charlton–Camden county line.

SR 40 enters Kingsland on King Avenue, which has a grade crossing of the First Coast Railroad and intersects US 17/SR 25 (Lee Street).

SR 40 expands again to a five-lane road with center turn lane in the vicinity of the Kingsland Fire-Rescue headquarters and then a six-lane divided highway as it begins to closely parallel the St. Marys Railroad through a commercial area just west of its partial cloverleaf interchange with I-95.

[6][7] Near the east end of the commercial area on either side of I-95, SR 40 becomes a five-lane road with center turn lane.

SR 40 intersects a branch of the railroad that heads into the naval base, crosses a bridge over Dark Entry Creek before meeting the southern end of SR 40 Spur (Charlie Smith Sr. Highway), which heads north along the western edge of the naval base on its way to Crooked River State Park.

[13] SR 40 was under construction along its present alignment from US 17 in Kingsland to the south end of Osborne Street in St. Marys by October 1934; the highway was completed as a paved road by January 1936.

[21][22] The first major rerouting of SR 40 occurred between 1963 and 1966 when the highway was moved to its present alignment between the Charlton–Camden county line and Kingsland.

SR 40 Connector heads east from the U.S. highways as a two-lane road that passes Charlton County High School.

The highway continues southeast and intersects SR 252, which heads west towards downtown Folkston and east towards White Oak in northern Camden County.

North of its oblique intersection with Colerain Road and Douglas Drive, the spur route expands to a controlled-access divided highway and serves as the western boundary of Naval Submarine Base Kings Bay.

North of the latter junction, SR 40 Spur reduces to two lanes and has a grade crossing with the branch of the St. Marys Railroad that enters the naval base.

SR 40 Spur leaves the edge of the base as it enters Crooked River State Park.

The highway reaches its northern terminus at the park gate a short distance south of the Crooked River.