John Carter's arrival aboard the Safety in 1635 was the beginning of an illustrious career dedicated to the establishment of Colonial Virginia. Beginning in 1641 he represented Upper Norfolk-Nansemond County in the House of Burgesses, and in 1653 was appointed to represent Lancaster County where he had established his plantation, "Corotoman." He served as a member of the Governor's Council, Colonel in the militia, county court justice, and was prominent in the affairs of Christ Church.

John Carter married five times and fathered several children, but at his death in 1669 only his sons, John II and Robert, and daughter, Elizabeth, survived him. Robert "King" Carter, whose name is synonymous with Colonial Virginia and through whom John Carter I became progenitor of an elite aristocracy, inherited "Corotoman" in 1690 when his elder brother died without heir.

In 1702 Robert Carter was appointed agent of the Fairfax Proprietary and in this position amassed immense wealth and land holdings of more than 300,000 acres. His death in 1732 was premature to the completion of his greatest tangible legacy, the magnificent architectural treasure known as Historic Christ Church in Lancaster County.