For three years after his marriage to Mary Forth, John Winthrop lived on the Groton estate, learning how to manage real estate, collect rents and levy fines against tenants. His father, Adam Winthrop, Jr., wanted to ensure that the young Winthrop could manage the manor before he turned over the family's estate to him. Winthrop worked hard, but in order to keep true to his Puritan faith, he restrained himself from getting caught up in the work or the material rewards it offered.

Tragedy struck the Winthrop household in June of 1615, when John's wife of ten years, Mary, died. Winthrop soon married Tomasine Clopton, who died one day after their first wedding anniversary. The deaths in such proximity took a toll on Winthrop, who did not remarry for two years. However, in 1618, he married Margaret Tyndal, who would be his partner and correspondent through the next three decades, including their seventeen years in the New World. Margaret fit Winthrop's lifestyle better than his first two wives, since as a devoted Puritan she understood his motivations and concerns.

Winthrop began to study the law in addition to his work on the manor. Some historians suggest that his duties as head of the manor did not keep him fully occupied, and he entered law so that he would not have more free time than a man of true Puritan faith could rightfully claim. When Winthrop turned eighteen, the age of majority, he was appointed a justice of the peace–as was customary for nobles at the time. Three years later, in 1609, his father's diary remarks on how well Winthrop handled his first court at Groton. At the court, usually held every three to four weeks, the manor's tenants could lodge complaints and sue each other, and it served as great practice for Winthrop as he became more involved in the legal proceedings of his estate and England.

In 1613, Winthrop entered the famous Gray's Inn, one of the burgeoning law schools in London. Few of the Inns of Court, as they were called, were as well respected as Gray's; Francis Bacon had studied at Gray's in the late sixteenth century, as had the admiral who defeated the Spanish Armada. By 1617 he had returned to Suffolk to practice as a justice of the peace. Since his father had retired from the estate, its operation became entirely the responsibility of John Winthrop. The family estate had grown considerably with the dowries from John Winthrop's wives, and John was left better off than his father. In addition to his extensive estate duties, he began sitting in on trials as justice of the peace. The quarterly county court brought Winthrop into contact with every sort of criminal case short of treason.

As he advanced through the courts he began to be exposed to England's parliamentary machinery, and he became more involved in England's affairs. In the 1620s, he served as counsel to a committee in parliament to help develop legislation. The work in the courts brought him into constant contact with members of Parliament and other influential countrymen.

His legal career took another step forward when, in 1626, Sir Robert Naunton appointed him to serve as an attorney for the Court of Wards and Liveries, which oversaw cases pertaining to inheritance and underage heirs whose land was handled by the court until the heir reached the age of maturity. The court was notoriously corrupt, often renting an estate out to businessmen who pillaged and stripped the estate bare long before the rightful heir could take over. Even more so, every person appearing before the court had to retain one of the court's attorneys to argue the case–either Winthrop or one of the other two lawyers–leading to a very steady income for the lawyers.

The long separations from his wife and family saddened Winthrop–the new court met quarterly for up to seven weeks at a time–and he briefly considered moving his family to London or its suburbs, but he could not locate an appropriately lavish house. His loneliness, coupled with his growing disdain for the corruption in the English government, began to make him restless. He believed that because of its injunction to live "in this world," Puritanism would allow–if not force–him to improve conditions around him. As the 1620s ended, Winthrop and his fellow Puritans began to take stock of the wickedness and dishonesty surrounding them. They did not like what they saw.

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