Career
Carter represented his family's business interests in London during his time in England, and acted as his father's agent with Perry, Lane and Company. He was also admitted to the Inns of Court in 1722. Governor Spottswood with the concurrence of his Advisory Council (of which his father was a leading member) recommended Carter as solicitor of Virginia affairs in England on June 23, 1722, and this John Carter held that position for about a year until he returned to Virginia.
For 1500 pounds sterling Robert Carter bought an appointment for his firstborn son as secretary of the Virginia colony. John Carter received the appointment on June 21, 1722, and returned to Virginia that winter. The secretary's office, generally held for life at the time, was politically powerful as well as lucrative. Not only did the secretary keep the colony's records, he earned fees for more than sixty different services (especially recording land patents but also issuing writs for election of burgesses), as well as appointed all of the clerks for the county courts (and received part of the fees that each clerk received in lieu of a salary). By the time of his death, the position probably earned John Carter about 1,800 pounds sterling annually.
When a vacancy occurred on the Governor's Advisory Council, his father's influence helped John secure the lifetime appointment, on January 29, 1724, and they served together on the council for nine years. At his third Governor's Council meeting, John received a 6,000-acre tract of land on the north branch of the James River adjoining land of Col. Thomas Randolph, then in Goochland County, which later was split into Albemarle, Nelson and Amherst Counties. The following year, John Carter patented 9,350 acres in Albemarle County from the foot of Monticello Mountain south to the Hardware River (about 10 miles), and secured that land by building a mill and a road (later called the "Secretary's Road" across the "Secretary's Ford" of the Rivanna River, to the town of Bremo on the James River), as well as a claim house he named Clear Mount on the eastern side of what would be called "Carter's Mountain", and which his son Edward Carter would rebuild and name "Blenheim" in honor of the Duke of Marlborough's defeat of the Prussian army in Blenheim, Belgium in 1704. This John Carter would secure another 10,000 acre grant in Amherst and Nelson counties near the Piney and Buffalo Rivers in 1738.
From the time of his marriage in 1721 until his own death in 1742, John Carter lived at and managed the Hill family's Shirley Plantation on the James River, most believe with his father-in-law until that man's death sometime between 1721 and 1726. Shirley Plantation was much closer to the colonial government offices in Williamsburg. Furthermore, other powerful and intermarried families were nearby: the Byrd family at Westover Plantation and the Harrisons at Berkeley Plantation. Also, upon his father's death 1732 as discussed below, through primogeniture this John Carter inherited considerable property, including Corotoman plantation and hundreds of enslaved workers, as well as a mercantile business in Lancaster County that also traded West African slaves obtained from Liverpool merchants Samuel Powell and Foster Cunliffe. John Carter then divided his time between Shirley and Corotoman plantations, as well as a townhouse in the colonial capital, Williamsburg. His father's new mansion at Corotoman had burned a few years before his death and was not rebuilt, perhaps in part because the "Old House" had not been torn down and because of ongoing building projects on the other plantations discussed below, as well as Christ Church that his father had started. His wife Elizabeth wrote about the difficulties of moving her children and household between those locations, and by 1739, with most of his father's estate settled, this John Carter settled permanently at Shirley and left Corotoman in the hands of a reliable overseer. But John Carter's plantations inherited and acquired included 20,000 acres in Lancaster County, 6,000 acres in Essex county, 6,000 acres in Prince William counties (including tracts on Cedar Run, Broad Run and 10,000 acres on the Occoquan River), additional acreage in Richmond and Westmoreland and Northumberland Counties, and the lease of most of the Northern Neck Proprietary.
However, the Carter family's power and wealth concerned some, including Lieutenant Governor Hugh Drysdale, who raised concerns with the Board of Trade in London. Despite Drysdale's death, the Board of Trade's inquiry in 1727 prompted Carter to defend the perquisites of his office, as well as his own conduct. Although he was not removed from either office, Carter failed to secure another lucrative post he sought that year, as deputy auditor of the royal revenue in the Virginia Colony.
After 1732, John Carter not only managed his father's enormous estate of 300,000 acres, more than 1,000 slaves and 10,000 pounds sterling (with his half brothers Landon of Sabine Hall and Charles of Cleve as co-executors), he also managed Ripon Hall on the York River, which was inherited by his young half-brother George, and was the executor of the estate of his late half-brother Robert (which included Nomini Hall and was inherited by the then-underage Robert Carter III), and the estate of his late brother-in-law Mann Page (Rosewell Hall, where his sister and co-executor Judith lived), and that of his sister Elizabeth's husband Dr. George Nicholas. Thus this John Carter raised Robert Carter Nicholas, orphaned in 1734. King Carter's will also appointed John Carter to inherit the agency relationship with the Fairfax and collect quitrents for the Northern Neck Proprietary. However, in England, the Northern Neck Proprietary's owner, Lord Thomas Fairfax had other ideas, and in 1733 appointed his nephew William Fairfax (then collector of customs of the Massachusetts colony) as his agent, and in 1735 Lord Fairfax arrived in Virginia, and John Carter paid his quitrents.
Beginning the 1723, Secretary John Carter erected an elegant plantation house at Shirley, which was completed in 1738 and remains today. By the time of his death, this John Carter owned 52,000 acres of land. As was also common among the colony's ruling families of the era, Carter also raced thoroughbred horses and attended cockfights, presumably gambling on most of such events.
In his early forties, by 1741, Carter's health began to decline. He last attended the Governor's Council on November 3, 1741. During late 1741, Carter reportedly suffered from "Dropsy in the Belly". Either that illness worsened or another malady struck by July 1, 1742, when John Carter executed his (now-lost) last testament.