Generally, when an area became part of an independent city, through annexation, merger, consolidation, or conversions, the secondary roads passed from the state system to local responsibility.

This arrangement eventually led to new conflicts over ownership and responsibility for the c. 1928 Kings Highway Bridge across the Nansemond River on State Route 125, which was closed in 2005 by the VDOT for safety reasons.

The state's secondary roads system had also grown by 30% from its original size, despite the large geographical areas (and miles of roadway) lost over the years to expanding and additional independent cities and incorporated towns.

However, despite the VDOT's (and its predecessor agencies) accomplishments, the relationship between the counties and the state highway officials since 1932 has always been somewhat strained.

Under the Code of Virginia, as amended, "The Boards of Supervisors or other governing bodies...shall have no control, supervision, management, and jurisdiction over...the secondary system of state highways" (§33.1-69).

Late in the 20th century, the problems inherent in this arrangement became especially apparent with regards to the secondary roads system in many fast-growing suburban counties outside incorporated towns and cities.

A state-sponsored study in 1998 focused on 14 of the fastest-growing counties identified such issues as drainage, speed limits, and planning and coordination of roads with development as those local leaders felt should be within their ability to control, while the authority to do so was in fact, held by a state agency instead.

"[6] In the early 21st century, the Virginia General Assembly was considering legislation to allow some counties to choose to resume control and care for the secondary highways within their boundaries.

James City County, with a population that grew by 56% between 1980 and 1990 according to the 1998 VDOT study, was reported by the local news media to be under consideration for a pilot project of this type.

The lack of progress in such reform, however, has prompted many residents and businesses of Fairfax County—the state's most populous and congested county—to push for cityhood, to retain a greater share of fuel tax revenues.

Those that maintain their own streets, including most primary routes, are as follows: Abingdon, Ashland, Big Stone Gap, Blacksburg, Blackstone, Bluefield, Bridgewater, Christiansburg, Clifton Forge, Culpeper, Farmville, Front Royal, Herndon, Lebanon, Leesburg, Luray, Marion, Orange, Pulaski, Richlands, Rocky Mount, South Boston, South Hill, Tazewell, Vienna, Vinton, Warrenton, Wise, Wytheville In the following towns, all primary routes are maintained by the state, but other streets are town-maintained: Altavista, Chase City, Chincoteague, Dumfries, Elkton, Grottoes, Narrows, Pearisburg, Saltville, Smithfield, Strasburg, Woodstock Many, but not all, secondary routes in Virginia are streets and unpaved country roads that are mostly short in nature.

[1] Virginia includes 51.12 miles (82.27 km) of toll roads maintained by other entities, typically through public-private partnerships.