Over the second half of the 1630s, the Massachusetts Bay Colony had an on-again, off-again war with the nearby Pequot Indians. Raiding parties of both colonists and Indians attacked each other's settlements, leveling small isolated settlements and killing traders. Unfortunately for the Indians, they were outnumbered, and the war was merely a war of attrition for them. Strangely enough, during the war, Roger Williams found a link to the colony he had never possessed earlier. Massachusetts Bay repeatedly sent soldiers and supplies to Williams's fledgling colony at Narragansett Bay to help defeat the Indians in his area. However, the most lethal weapon in the settlers' arsenal was smallpox. The Indians, never having been exposed to the disease before, had no immunity built up. The disease took a horrible toll on the tribe, and by 1640 the tribe practically had been wiped out.

With the colony firmly established, both physically and spiritually, the people of the colony began to turn their attention to improving the civil governance of the colony.

In 1639, a group of newly arrived immigrants began agitating that Winthrop's continued service as governor gave rise to the potential for despotism, such as was prominent back in England. While the group personally liked Winthrop, their point was a more general one than one carried out of dislike for the governor. They just wanted to ensure that no governor–Winthrop or otherwise–would get carried away with the post and declare himself governor for life. The movement quickly took on a life of its own, to the point that many colonists believed that someone had hatched a plot to install a governor for life. The settlers began to prepare to oust Winthrop at the next election, and by a narrow margin Thomas Dudley was reelected to the governor's post. The following year Richard Bellingham again beat Winthrop by a mere six votes.

When Dudley assumed office he set about building a uniform criminal code for the colony, a project that had been on the back burner for several years. Winthrop and the other deputies had been reluctant to develop the code for two reasons. First, they wanted a code to develop a series of legal decisions, instead of being laid down in whole by the legislature. After all, most Englishmen recognized that common law was better than laws passed by Parliament, as common law ensured that God's will was being followed. Second, and perhaps more importantly, the colony's charter forbade it to pass laws different from those in England–but much of the common law developed in Massachusetts Bay was diametrically opposed to English law because of the colony's Puritan beliefs. However, Dudley believed that the codification of the colony's common law was crucial to its continued survival. Thus, he appointed Nathaniel Ward to draw up a code. Ward's code, named the Body of Liberties, stood as a Magna Charta for the Massachusetts Bay colony and covered more than a hundred provisions–dealing with everything from the rights of magistrates and churches to the rights of servants and animals. It also reasserted many of the rights that freeman had sought over the colony's first decade, like that of the freemen to elect deputies. To prevent the recurrence of problems like those caused by Anne Hutchinson and Roger Williams, the code allowed the General Court to impose punishments on any member of a church, irregardless of position. After hours of debates and revision, the colony adopted Ward's Body of Liberties in December of 1641. Winthrop recorded its passage in his journal without elaboration.

In the early 1640s, Winthrop was hit by one of the few personal crises of his time in New England. Since he had devoted most of his first decade in Massachusetts Bay to organizing the state and his role as governor, he had delegated control of his personal lands and estates to James Luxford. However, Winthrop discovered that–more out of incompetence than spite–Luxford had run up debts of hundreds of pounds on Winthrop's land and had almost bankrupted Winthrop. However, in a sign of their appreciation for Winthrop's work, the colony rallied around him. The General Court offered his family another three thousand acres of land, and a collection in Boston netted more than five hundred pounds for the Winthrop family.

The only other major incident for Winthrop in the 1640s involved two Frenchmen who both claimed to govern the French colony of Acadia: Charles de Saint Etienne de la Tour and Charles de Menon, who became know in New England as La Tour and D'Aulnay respectively. D'Aulnay was the more dangerous to the English. Winthrop sided with La Tour, realizing that although he despised both men and their religion, he should align himself with the lesser of the two evils to help the colony. Any such alliance did not sit well with the rest of the colony, however, and Winthrop was censured by the court for his too "lenient" treatment of La Tour.

In the summer and fall of 1648 the colony republished Ward's Body of Liberties and included subsequent decisions by the General Court. The new code, coupled with a synod of area ministers–in which they drew up a formal document explaining the governance and organization of the congregational church–presented the colony with a formal system of governance and operation. Civil government stood ready for next challenge.

Unfortunately, in the winter of 1949, John Winthrop found himself in failing health. Beginning in February, 1649, Winthrop was bedridden. He died in his sleep on March 26, 1649 at the age of sixty-one. His colony, though, would thrive and prosper for many years to come.

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