Virginia's first known capital was Werowocomoco, the "seat" of the Native American chief we know today as Powhatan. Werowocomoco was located on modern Purtan Bay, on the north bank of the York River in Gloucester County, 10 miles upstream from Yorktown.
According to John Smith1, Pocahontas came to his rescue there. Now the government of the Pamunkey tribe, including the chief and council, is centered on a reservation upstream on the Pamunkey River, in King William County. The Mattaponi reservation is also upstream on the northern edge of King William County, and on the Mattaponi River.
When the English arrived in 1607, most werowances (lesser chiefs) in Tidewater were subordinate to a paramount chief named Powhatan (also known by other names, including Wahunsunacock). He had initially inherited control of six tribes located near modern-day Richmond and Ashland. In addition to control over the town of Powhatan located near today's Church Hill at the falls of the James River, Powhatan inherited authority over the Arrohothateck, Appamattuck, Mattaponi, Pamunkey, and Youghtanund.2 Over time, and before the English arrived, Powhatan gained control over the tribes living along the protein-rich York River where he would establish his capital at Werowocomoco, which meant "king's house."3

Werowocomoco was never the capital of all Virginia. It was the capital of the Algonquian confederation ruled by one paramount chief who controlled only a portion of Tidewater Virginia, mostly between the southern bank of "Powhatan's river" (today's James River) and the Potomac River near Aquia. Each werowance who owed allegiance to Powhatan had his own town site, identified by John Smith in his Map of Virginia.
The Iroquian-speaking Nottaways and Meherrins south of Powhatan's river (today's "James River"), and the Siouian-speaking Monacans and Manahoacs upstream of the falls on the Tidewaters rivers, owed no allegiance to Powhatan. Other Algonquian-speaking tribes north of the Rappahannock River, such as the Dogue, did not consider Powhatan to be their paramount chief - and until the English arrived, the Chickahominy tribe was allied with but not conquered by him.

Powhatan abandoned Werowocomoco in 1609 and moved his capital to Orapakes, to get further away from the English colonists.