DE 404, along with MD 404, serves as a major route connecting the Chesapeake Bay Bridge and the Baltimore–Washington Metropolitan Area with the Delaware Beaches.

From the state line, the route heads southeast on two-lane undivided Seashore Highway, passing through a mix of farmland and woodland with some homes and businesses.

The route briefly becomes a divided highway before it turns northeast onto two-lane undivided Newton Road, with DE 404 Bus.

Upon reaching an intersection with US 13 Bus./DE 404 Bus., DE 404 splits from US 13 by heading southeast onto four-lane divided Seashore Highway.

The road passes a few businesses before becoming two lanes and undivided as it continues through agricultural areas, coming to an intersection with DE 18.

DE 18/DE 404 enters the town of Georgetown and becomes Bridgeville Road, running to the north of the Jack F. Owens Campus of Delaware Technical Community College.

The road intersects US 113 and the western terminus of DE 404 Truck in a commercial area and continues east.

[3][4] At this point, DE 404 continues northeast concurrent with US 9 on East Market Street through the downtown area.

The road crosses the Delmarva Central Railroad's Indian River Subdivision line at-grade and runs through residential areas with a few businesses, passing south of the Southern Delaware Tourism Visitors Center.

Following this intersection, US 9/DE 404 passes through more rural land, reaching a junction with DE 5 near businesses in the community of Harbeson.

[3][4] DE 404 serves as part of a major route connecting the Chesapeake Bay Bridge and the Baltimore–Washington Metropolitan Area to the Delaware Beaches.

[5][6] DE 404 also serves as part of a primary hurricane evacuation route from the Delaware Beaches to points inland.

[1] All of DE 404 is part of the National Highway System,[10] a network of roads important to the country's economy, defense, and mobility.

[11] By 1920, what would originally become DE 404 was an unimproved county road, with the section east of Bridgeville under contract as a state highway.

[18] A traffic study on increasing congestion along east–west roads in Sussex County, including DE 404, was undertaken in 1986 in coordination with Maryland officials.

[19] In 1988, plans were made for a consultant to design road improvements for an east–west corridor between Bridgeville and the Lewes area.

In March 2021, five virtual workshops on the study were held to present collected data and gather input from the public.

The project was intended to improve safety at the intersection, which saw a high accident rate due to its design.

Work on the project was completed on May 21, 2009, with DelDOT secretary Carolann Wicks and President of Commissioners for the Town of Bridgeville William Jefferson in attendance at a ceremony.

The route begins at DE 404 northwest of Bridgeville, heading southeast on two-lane undivided Seashore Highway through agricultural areas with some homes.

enters Bridgeville and heads through commercial areas, briefly becoming a divided highway before it intersects Federalsburg Road.

The route begins at the intersection between US 113 and DE 18/DE 404, heading south along with US 113 on four-lane divided Dupont Boulevard.

The road passes through a mix of farmland and woodland with some development, coming to a roundabout with South Bedford Street, where the name changes to Park Avenue.

The routes continue east before curving to the northeast, crossing the Delmarva Central Railroad's Indian River Subdivision line at-grade.

The road turns east and passes to the south of Delaware Coastal Airport, where it makes a curve to the north.