Large parts of it were built on the former right-of-way of the Overseas Railroad, the Key West Extension of the Florida East Coast Railway.

[16][17] US 1 then crosses to and traverses Long Key, which is mostly unincorporated except for the city of Layton, which the highway passes through.

Immediately the Overseas Highway enters Tavernier,[20] where it temporarily splits into a pair of one-way roads through the community.

US 1 swings to the northwest, forms the southern boundary of North Key Largo,[23] and becomes a two-lane divided road after the intersection.

[29] Construction on the original Overseas Highway, designated State Road 4A (an extension of a route running from Miami to Homestead), lasted through most of the mid 1920s.

Funding would eventually come through the Federal Emergency Relief Administration, a program established by President Franklin D. Roosevelt's New Deal.

Hundreds of disgruntled World War I veterans seeking early payment of wartime pensions were employed for construction on the roadway and bridges as part of a government relief program.

The hurricane caused widespread damage throughout the area and destroyed much of the Overseas Railroad in the upper keys.

[31] Just west of Lower Matecumbe Key at Mile Marker 73 on the current highway, eight concrete bridge piers and a small dredged island are all that remains of the veterans' work.

[32] After the hurricane, the Florida East Coast Railway was financially unable to rebuild the damaged sections of the Overseas Railroad.

Seizing a rare opportunity, the state purchased the railroad's entire right of way south of Florida City and its remaining infrastructure for a price of $640,000.

[33] The railroad's bridges, which withstood the hurricane and were in good condition, were retrofitted with new two-lane wide concrete surfaces for automobile use.

The conversion of the railroad bridges to automobile use was accomplished by Cleary Brothers Construction Co. of West Palm Beach.

Pigeon Key, roughly the midway point of the Seven Mile Bridge, served as the headquarters for the "Overseas Road and Toll District.

This resulted in completing the rest of the highway throughout the keys on the former railroad right of way, which the state owned and was a more direct route with smoother curves that would allow for higher speeds.

Also included in this project was the construction of the highway from Florida City to Key Largo on the old railroad route via Jewfish Creek.

Remnants of the wooden bridge at Tarpon Creek on Upper Sugarloaf Key still remain, which was destroyed by a fire in later years.

In recent years, Pigeon Key was used by the University of Miami as an oceanography laboratory, but current efforts to restore the buildings on the island have resulted in the establishment of a railroad museum there.

Upon completion, the FKOHT will include an integrated system of educational kiosks, roadside picnic areas, scenic overlooks, fishing piers, water access points, and bicycle and jogging paths.

The development of the trail will provide a mechanism for the preservation and use of the historic Flagler Railroad Bridges, 23 of which still exist and are mostly intact.

In all cases, original bridgework will be repaired or rebuilt, and the breaks created during the 1980s and 1990s fishing pier conversion will be reconnected.

[45] Mileposts are taken from US 1, which begins approximately 4 miles (6.4 km) south at an intersection with Whitehead and Fleming streets in Key West.The entire route is in Monroe County.