U.S. Route 17 in Georgia runs north–south near the Atlantic Ocean, serving Brunswick and Savannah on its path from Florida at the St. Marys River to South Carolina at the Savannah River. Except for part of the route in Savannah, which runs along State Route 404 (Interstate 16) and State Route 404 Spur to the Talmadge Memorial Bridge to Hutchinson Island, US 17 is also State Route 25. SR 25 uses an older western alignment of US 17 into South Carolina.

All of US 17 in Georgia that does not have a local street name is known as Ocean Highway (alternatively spelled Ocean Hiway), which was the name of an auto trail established in 1935 connecting New York with Jacksonville. The Georgia General Assembly made the Ocean Hiway designation official in a 1958 resolution that recognized the concerted advertising effort of the Ocean Hiway Association, its impact on tourism, and the signage of the highway in the coastal states to the north. US 17 runs concurrently with SR 25 for almost its entire length in the state. The highways split at the I-16–I-516 interchange in Savannah; US 17 follows I-16 and its unsigned companion SR 404 and then signed SR 404 Spur to the South Carolina state line at the Savannah River while SR 25 heads northwest along the old route of US 17 to Port Wentworth to cross the river upstream from the city. US 17 is a part of the National Highway System from US 82, SR 520, and SR 303 south of Brunswick to US 341 in Brunswick, and from its southern interchange with I-516 to the South Carolina state line.

US 17 enters Camden County, Georgia from Nassau County, Florida by crossing the St. Mary's River on a through truss bridge. The two-lane highway closely parallels the First Coast Railroad, formerly part of the Seaboard Air Line Railroad (now CSX Transportation) through the southern part of the count. US 17 crosses Catfish Creek before entering the city of Kingsland. The U.S. Highway passes through the city as Lee Street, which intersects the St. Mary's Railroad at its junction with the First Coast line just south of SR 40 (King Street), which parallels the railroad east to St. Marys. Leaving Kingsland, the highway intersects a spur from the rail line and crosses the main flow and the North Fork of the Crooked River. US 17 parallels the First Coast Railroad to its terminus at the hamlet of Seals. The highway passes through Colesburg before entering the city of Woodbine, the county seat of Camden County. Within the city, US 17 follows four-lane divided Bedell Avenue, which intersects SR 25 Spur (10th Street), a connector between the center of town and I-95. The highway intersects and begins to run concurrently with SR 110 (4th Street) within the Woodbine Historic District. US 17 and SR 110 reduce to two lanes and leave town by crossing the Satilla River.

US 17 and SR 110 cross Piney Island Creek and meet the eastern end of SR 252 (Burnt Fort Road) at the hamlet of White Oak just south of White Oak Creek. The U.S. Highway and state route cross Waverly Creek then diverge at Waverly. US 17 curves east and enters Glynn County by crossing the Little Satilla River at Spring Bluff. The U.S. Highway curves north and within a suburban area has a four-way intersection with US 82, SR 520, and SR 303. SR 303 heads north as Blythe Island Highway and US 82 and SR 520 head west as South Georgia Parkway. US 17 turns east onto four-lane divided South Georgia Parkway, here also known as Jekyll Island Road, to run concurrently with US 82 and SR 520. The concurrency with US 82 ends at that highway's eastern terminus at a partial cloverleaf interchange with I-95. US 17 and SR 520 cross Fancy Bluff Creek onto Colonel's Island and the highway becomes undivided at its crossing of the Golden Isles Terminal Railroad between a pair of automobile manufacturing plants. The highway becomes divided again shortly before SR 520 splits east as Jekyll Island Road toward Jekyll Island as US 17 curves north to cross the Brunswick River on the cable-stayed Sidney Lanier Bridge into the city of Brunswick.

US 17 heads along the eastern edge of Brunswick as Glynn Avenue, a controlled-access four-lane divided highway that has junctions with the southern termini of US 341 (4th Avenue) and US 25 (Gloucester Street), the latter of which is also SR 25 Connector. The highway gains a third lane southbound at US 25 and a third lane northbound at the F.J. Torras Causeway to St. Simons Island, which is unsigned SR 25 Spur E. US 17 crosses Cypress Mill Creek and leaves the city limits just south of its directional intersection with SR 25 Connector (Golden Isles Parkway), which connects US 17 with I-95. There is no direct access from southbound SR 25 Connector to northbound US 17; that movement is made via the U.S. Highway's junction with the eastern end of SR 303 (Cypress Mill Road). The U.S. Highway continues north with four lanes through a suburban area north of Brunswick. US 17 reduces to two lanes just north of Chapel Crossing Road to the east of the Federal Law Enforcement Training Center. The U.S. Highway re-enters a rural area as it passes to the east of Brunswick Golden Isles Airport. US 17 begins to run concurrently with SR 99 and I-95 Business and runs along the edge of the Hofwyl-Broadfield Plantation Historic Site before crossing the South Altamaha River into McIntosh County.

US 17, SR 99, and I-95 Business pass through the Altamaha Waterfowl Management Area, during which the highways traverse Champney Island, Butler Island, and Generals Island. The highways cross between the islands by crossing the Champney River and the Butler River, which are branches of the Altamaha River, and the Darien River, where the highways enter the city of Darien, the county seat of McIntosh County, as Walton Street. In the center of town, SR 99 splits east onto Adams Street and US 17 continues as North Way, which is a four-lane undivided street in the city. North of the city limits, I-95 Business splits west along SR 251 and the U.S. Highway reduces to two lanes and passes Eden Field Airport. US 17 crosses a pair of swamps around the hamlet of Ardick and intersects SR 99 (Ridge Road) again at Eulonia. The highway crosses the Sapelo River and Buck Hill Swamp on its way to its crossing of the South Newport River at South Newport.

US 17 continues north through Liberty County and meets I-95 at a diamond interchange. The highway enters the sparsely populated city of Riceboro at Payne Creek. US 17 temporarily expands to four lanes between its crossing of the Riceboro Southern Railway, which is part of the former Seaboard Air Line corridor, and its junction with the eastern end of SR 119 (E.B. Cooper Highway). At the north end of town, the highway crosses Riceboro Creek. US 17 crosses Peacock Creek and enters the city of Midway at Porter Creek. US 17 intersects US 84 (Oglethorpe Highway) in the center of town. The U.S. Highway expands to a four-lane divided highway at its intersection with SR 196 (Leroy Coffer Highway) just before crossing Mount Hope Creek, a tributary of the Jerico River, at the Liberty–Bryan county line. US 17 enters a suburban area and parallels the city limit of Richmond Hill, which is immediately to the west, until the highway fully enters the city just before its partial cloverleaf interchange with I-95. The U.S. Highway crosses over CSX's Nahunta Subdivision and intersects SR 144 (Ford Avenue) before leaving the city and entering Chatham County by crossing the Ogeechee River at Kings Ferry.

US 17 continues northeast as Ogeechee Road through a suburban area. The U.S. Highway meets SR 204 (Abercorn Expressway) at a diamond interchange in the suburb of Georgetown then crosses the Little Ogeechee River. US 17 meets the southern end of SR 307 (Dean Forest Road) just west of Salt Creek, then continues east as a five-lane road with center turn lane. The highway crosses over CSX's Nahunta Subdivision before reaching I-516 and SR 21 (W.F. Lynes Parkway) at a diamond interchange the city limit of Savannah. Ogeechee Road continues toward downtown Savannah as US 80; both U.S. Highways head north from the interchange on four-lane I-516. The freeway has a partial interchange with Tremont Street (southbound exit, northbound entrance), which serves the Savannah Amtrak station, and crosses CSX's Savannah Subdivision before its junction with I-16 (Jim Gillis Historic Savannah Parkway). US 17 heads east on six-lane I-16 while US 80, SR 21, and SR 25 continue north concurrent with I-516.

I-16 and US 17 have a partial interchange with the northern end of SR 204, then curve northeast. The U.S. Highway diverges from I-16 one interchange west of the Interstate's eastern terminus and just south of a partial interchange (northbound exit, southbound entrance) with Gwinnett Street. Four-lane US 17, which is also signed as SR 404 Spur, passes through another pair of partial interchange: a northbound exit and southbound entrance for Louisville Road and southbound exit, northbound entrance for a spur to Oglethorpe Street. North of the latter interchange, US 17 ascends onto the cable-stayed Tallmadge Memorial Bridge, which crosses over Bay Street and the main channel of the Savannah River. The U.S. Highway descends onto Hutchinson Island, crosses over Wayne Shackelford Boulevard and the Savannah Port Terminal Railroad, and has a partial cloverleaf interchange with the boulevard, which leads to the Savannah Convention Center. Within the interchange, US 17 reduces to two lanes and crosses the Back River, another branch of the Savannah River, on a low-level bridge into Jasper County, South Carolina.

In the early 1920s, SR 25 initially ran only from Sterling south to Brunswick and north into Savannah and South Carolina; State Route 27 continued south from Sterling (initially along present State Route 99 and Haynor Road north of Waverly) into Florida. US 17 was designated along the route in 1926, and by 1930 the whole route was SR 25.

The Talmadge Memorial Bridge opened in 1953, carrying State Route 25 Alternate and U.S. Route 17 Alternate over the Savannah River into South Carolina. In 1994, US 17 Alternate was eliminated, and US 17 was rerouted over it.

The section of US 17 known as the "Gateway to Historic Brunswick and The Golden Isles" was included in The Georgia Trust for Historic Preservation's 2006 list of Places in Peril.

Georgia State Route 25 is US 17's companion route along much of the U.S. Highway's course through Georgia. The state highway has a total length of 129.07 miles (207.72 km); the highway runs concurrently with US 17 for 119.56 miles (192.41 km) from the Florida state line near Kingsland north to Savannah. SR 25 has a length of 9.51 miles (15.30 km) from its split with US 17 in Savannah to the South Carolina state line near Port Wentworth.

SR 25 splits from US 17 at the I-16–I-516 interchange in Savannah. US 17 heads east with I-16 (Jim Gillis Historic Savannah Parkway) toward downtown Savannah and the Talmadge Memorial Bridge. SR 25 continues north on I-516 (W.F. Lynes Parkway), a four-lane freeway that also carries US 80 and SR 21. The freeway has a half-diamond interchange with Gwinnett Street, which connects downtown Savannah with the Savannah Amtrak station. The interchange allows access to and from the south. After crossing a rail line belonging to the Savannah Port Terminal Railroad, SR 15, I-516, and SR 21 diverge from US 80 and meet the western end of SR 25 Connector at another partial interchange. The southern part of the interchange includes ramps from northbound SR 25 to Augusta Street and from Augusta Street to southbound SR 25; Augusta Street serves as a connector to Bay Street, on which US 80 heads west and SR 25 Connector heads east. The interchange also includes ramps from southbound SR 25 to SR 25 Connector, SR 25 Connector to northbound SR 25, and from northbound SR 25 to Lathrop Avenue, which serves an industrial area along the Savannah River.

Within the interchange with US 80 and SR 25 Connector, SR 25, I-516, and SR 21 curve northwest. The highways cross CSX's Charleston Subdivision and parallel Bay Street toward the northern terminus of I-516 at a partial cloverleaf interchange with Burnseed Boulevard on the boundary of the cities of Savannah and Garden City. SR 25 exits onto the four-lane connector between US 80 and Main Street; SR 21 continues northwest as the freeway transitions to Augusta Road, a four-lane divided highway. SR 25 turns northwest onto Main Street, a five-lane road with center turn lane, crosses a canal, and parallels a portion of the port railroad. The highway reduces to two lanes at its intersection with SR 21 Spur (Brampton Road), which heads into the Port of Savannah. SR 25 curves north as it crosses a pair of intersecting rail lines and passes between the port property to the east and a residential area of Garden City to the west.

SR 25 meets the northern end of SR 307 (Bourne Avenue) just after leaving Garden City. The highway continues as Coastal Highway into Port Wentworth, the site of the 2008 Georgia sugar refinery explosion. SR 25 meets the eastern end of SR 30 (Bonnybridge Road) before leaving Port Wentworth and curving east around the northern end of an industrial area. The highway crosses the Front River, the main channel of the Savannah River, on the Houlihan Bridge, a through truss swing bridge. SR 25 continues east across Onslow Island, crosses the Middle River, cuts through Argyle Island, then crosses the Little Back River into South Carolina. The highway continues as South Carolina Highway 170, which intersects US 17 south of Hardeeville.

Georgia State Route 25 Connector is a 1.08-mile (1.74 km) connector route from US 341 east to US 17 in Brunswick. The connector route begins at US 341 (Bay Street) where US 25 turns east from Bay Street onto Gloucester Street, which is the main east–west street through downtown Brunswick. The route runs concurrently with US 25 along a four-lane undivided street east through the downtown area, then enters a residential area after intersecting Martin Luther King Jr. Boulevard. US 25 reaches its national southern terminus and SR 25 Connector reaches its eastern terminus at their intersection with US 17 (Glynn Avenue) at the eastern end of the street grid opposite Glynn County's famous marshes.

Georgia State Route 25 Connector is a 3.11-mile (5.01 km) connector route between SR 25 and US 17 in Savannah. The route begins as Augusta Avenue at a half-diamond interchange with I-516, SR 21, and SR 25; the interchange allows access to and from the south. SR 25 Connector and US 80 run concurrently on four-lane Augusta Avenue to Bay Street, onto which US 80 heads west and SR 25 Connector heads east; the road continues north as Lathrop Avenue. East of the intersection, the connector route receives a ramp from the southbound freeway and has an exit ramp from the westbound direction to the northbound freeway. SR 25 Connector follows Bay Street, a four-lane undivided street, toward downtown Savannah. The street crosses over a portion of the Savannah Port Terminal Railroad before passing under the Talmadge Memorial Bridge. At the west edge of historic Savannah's street grid, SR 25 Connector turns south onto Martin Luther King Jr. Boulevard. The highway follows the four-lane undivided street to Oglethorpe Avenue, a four-lane divided street the highway follows west to its terminus at a partial interchange with US 17 and its companion route SR 404 Spur. The interchange allows access to and from the Talmadge Memorial Bridge to Hutchinson Island and South Carolina.

Georgia State Route 25 Spur is a 4.55-mile (7.32 km) spur route on the north side of Brunswick that serves to connect I-95 with the Golden Isles via US 17. The spur route, which is named Golden Isles Parkway, begins at a directional intersection with US 17 and SR 25 in the city of Brunswick. There is no direct access from southbound SR 25 Spur to northbound US 17 and SR 25; that movement is made via the spur's first intersection with SR 303 (Cypress Mill Road). The four-lane divided highway heads northwest as a controlled-access highway through a suburban area north of Brunswick. SR 25 Spur passes to the west of the National Law Enforcement Training Center and Brunswick Golden Isles Airport. The spur route reaches its northern terminus at a diamond interchange with I-95. Golden Isles Parkway continues as a county highway to its terminus at SR 99 (Grants Ferry Road).

Georgia State Route 25 Spur is a 2.79-mile (4.49 km) connector route from US 17 and SR 25 east to I-95 in Woodbine. The spur route begins at US 17 and SR 25 (Bedell Avenue) south of downtown Woodbine. SR 25 Spur heads east as two-lane 10th Street, which leaves the street grid and enters a rural, forested area. The route reaches its eastern terminus at the eastern edge of its diamond interchange with I-95. The road continues east as county-maintained Lang Road.

Georgia State Route 25 Spur E is the unsigned 4.13-mile (6.65 km) designation for the F.J. Torras Causeway, which serves as the only road connection between Brunswick and both St. Simons Island and Sea Island. The spur route begins at an intersection with US 17 (Glynn Avenue) northeast of downtown Brunswick. The highway heads east as a four-lane divided highway through the marshes on the east side of Brunswick. The F.J. Torras Causeway crosses the Back River, Little River, Mackay River, and Frederica River. After crossing the last river, which serves as part of the Intracoastal Waterway. the state highway alights onto Gascoigne Bluff on St. Simons Island and reaches its eastern terminus. The highway continues east as Frederica Road through the resort island.