It connects Park Presidio Boulevard (Hwy 1) in the Richmond District to US 101 on the Doyle Drive viaduct, and the Golden Gate Bridge.

When the Golden Gate Bridge opened in 1937, the approach for northbound traffic to Marin County was carried solely by Doyle Drive, from the east.

[10] The tunnel was made as long as possible without having to add forced ventilation to dilute carbon monoxide from automobile exhaust, and a 24-by-24-foot (7.3 by 7.3 m) shaft was built mid-way along the tunnel to provide passive ventilation, with the capacity to add a fan later for forced exhaust through the shaft, if necessary.

[13] Construction of the tunnel began in October 1938 and was complete by January 1940;[13] the Funston Avenue approach was dedicated for service on April 21, 1940.

[16] Delegates from British Columbia; the states of California, Oregon, and Washington; and the consul general of Mexico all attended and spoke at the dedication ceremonies.

[20] The top face of the south entrance to the tunnel is a popular target for graffiti vandals due to broken barbed-wire fences.