Carter was born probably at Corotoman, the Lancaster County plantation of his parents, Robert “King” Carter and his first wife, Judith Armistead Carter. His younger half brothers included(ca. 1707–1764), who represented King George County in the , and , who represented Richmond County in the assembly. Carter’s father, an extraordinarily successful merchant and planter and rising political figure, had high ambitions for him and sent him to England to be educated. Carter attended Mile End School, in London, entered the Middle Temple to study law in April 1713, and at age eighteen matriculated at Trinity College, University of Cambridge, on January 12, 1714. He became part of a small and frequently changing community of Virginians in London, most of whom were there on business or for their education. Carter lived very well in England and occasionally exceeded the £200 per year his father allowed him. A £50 bill from a tailor aggravated Robert Carter, who consoled himself that at least Carter had maintained a good character. “To have spent so much money upon a dunce or a blockhead,” his father admitted, would have been “most intolerable.” Like many other young gentlemen, Carter did not graduate from the university, but unlike many others, he completed his legal education and was called to the bar on May 27, 1720.
Carter represented his father’s business interests in London and briefly acted as the colony’s solicitor under an appointment from the lieutenant governor and Council. Carter’s father, who had become a leading member of the Council, purchased for him the patent for the office of secretary of the colony. Carter received his appointment on June 21, 1722, and that winter returned to Virginia. The secretary’s office, which he held for life, was both lucrative and politically powerful. The secretary was the colony’s record keeper. He appointed all of the clerks of the county courts and received from each a portion of the fees that the clerks were allowed in lieu of a salary. The secretary also earned fees from more than sixty different services, such as issuing writs for theand making out and recording land patents. By the time of Carter’s death, his annual income as secretary was estimated at £1,800. When a vacancy on the Council occurred in 1723, Robert Carter pressed to have John Carter named to that office, too, and on January 23, 1724, made the appointment. Father and son served on the Council together until the father’s death almost nine years later.
Although Carter was efficient and responsible in both offices, some men, including Lieutenant Governor, were concerned about the extent of the power of the secretary and perhaps worried about a potential for corruption if he retained the authority to appoint all of the county clerks. Drysdale mentioned his concerns to the Board of Trade, prompting Carter in 1727, not long after Drysdale’s death, to defend his conduct and the perquisites of the office. He asserted that he had not sold clerkships or illegally profited from his position. Secretaries of the colony retained the right to appoint county clerks and receive a portion of their incomes until the American Revolution (1775–1783). Carter remained ambitious, and later in 1727 he attempted to obtain appointment as deputy auditor of the royal revenue in Virginia, another influential and lucrative office, but that effort was unsuccessful. He held his seat on the Council and the position of secretary until his death.
Carter married Elizabeth Hill, of Charles City County, on October 3, 1723. They had one daughter, later the first wife of(1728–1777), and three sons, one of whom, Charles Carter, represented Lancaster County in the House of Burgesses. The marriage gave Carter and his wife ownership of Shirley plantation, which she inherited following the death of her father. Carter lived at Shirley until the death of his own father in 1732 and thereafter divided his time among Shirley, Corotoman, and a town house that he owned in Williamsburg. He was a busy man, especially after he and his half brothers undertook to administer their father’s enormous estate. Carter did most of the work, which occupied him until his death. His own estate demanded his close attention as well. By that time it consisted of about 52,000 acres of land, on which he raised tobacco and grain and where hundreds of tenants and slaves lived and labored. Carter also continued to operate his father’s mercantile concern in Lancaster County, and like his father he was a substantial .
Carter’s life epitomized the eighteenth-century Virginia elite. He held powerful and profitable public offices; he was related to many of the colony’s other leading families, among them Braxton, Burwell, Byrd, Harrison, Hill, Page, and Randolph; and he raced blooded horses, attended cockfights, and socialized with friends and neighbors. He also erected an imposing mansion at Shirley, an elegant plantation house that remains the property’s most famous landmark. Completed about 1738, it symbolized Carter’s status as one of the colony’s wealthiest gentlemen. Not long afterward, while Carter was still in his early forties, his health began to decline. He attended the Council for the last time on November 3, 1741, and was reported during that winter to be “very ill of the Dropsy in the Belly.” Carter signed his will on the following July 1 and died, probably at Shirley or in Williamsburg, on July 31, 1742. Most likely he was buried at Shirley or in the graveyard of the Westover Parish church.