The Jamestown colony flourished under the strict rule of John Smith. Nevertheless, The London Company (which was now called the Virginia Company) had formed a new government that was to be led by Thomas De La Warre. The new charter issued by the Virginia Company called for the appointment of a governor rather than a president. John Smith, who nearly died after igniting himself in a canoe, returned to England for good. Since De La Warre was unable to make the trip immediately, Thomas Gates was named interim governor. Unfortunately, Gates' ship wrecked off the coast of Bermuda and he was unable to resume the trip until new ships were built.

Meanwhile, the Virginia Company was in the process of reformulating its philosophy on potential profits in Jamestown. By 1609, it became obvious that profits would have to be realized over a long-term basis rather than immediately. The Virginia Company began reorganizing business possibilities to resemble those that had been successful in controlling the populations in Ireland. They proposed to bring England to the New World by sending families to Jamestown. Families were promised their own parcels of land for seven years of communal labor at Jamestown. This, the Virginia Company believed, would cause colonists to have a permanent stake in the welfare of the community as a whole, which would result in increased productivity and profit. Those that were not wealthy enough to pay their passage to the New World would have their trip subsidized (paid for) in exchange for seven years of labor. Those individuals became servants.

With John Smith out of the picture, and with the lack of a visible leader at Jamestown (because of Gates' shipwreck), Powhatan saw an opportunity to rid himself of the white settlers once and for all. Hence, Powhatan ordered his people to stop trading with the settlers. Without any leadership, and more specifically without the leadership of John Smith, the settlers once again became complacent and stopped contributing to the welfare of Jamestown. Trading teams that departed from Jamestown to Powhatan's lands rarely returned and were presumed dead. Without corn from the Algonkins, with settlers who refused to work, and with Powhatan's warriors seemingly closing in around them, the winter of 1609-1610 became known as the "Starving Time". Colonists were forced to eat cats and dogs and some were even executed for digging up human corpses to eat. When Gates finally arrived in 1610, only about 60 of the 500 settlers were still alive. Gates decided to abandon the settlement and nearly set sail with the remaining settlers for England. While Powhatan and his people celebrated wildly, Thomas De La Warre arrived with three fully supplied ships with a mission to stay indefinitely.

De La Warre and Gates re-established the tough discipline that had led the colony to success under John Smith. Under the set of rules developed by Gates and enforced by Sir Thomas Dale (the future governor of Virginia), settlers would be brutally punished for breaking the rules. Settlers were shot, burned at the stake, and hung at the gallows. Such transgressions as cursing carried physical torture or public humiliation as consequences.

During this time relations with the Indians worsened. The settlers were still dependent on the Indians for food, and became more and more violent in their quests to obtain it. The Indians, in turn, responded in kind, resulting in a bloody series of killings on both sides.

During the winter of 1612-1613, Samuel Argall devised a plan to kidnap Powhatan's favorite daughter, Pocahontas, who was visiting friends near Jamestown. Argall bribed two Indians with some copper kettles to lure Pocahontas onto an English ship. Although Pocahontas was suspicious, she boarded the ship and was kidnapped. Argall planned to ransom Pocahontas, but Powhatan was unwilling to meet the demands of the English. Negotiations dragged on for over a year, during which time, Pocahontas grew accustomed to life among the English. In captivity, she converted to Christianity, was baptized, and in 1814, married the wealthy tobacco planter John Rolfe. The marriage of Rolfe and Pocahontas resulted in a truce between the Indians and the English. Although Powhatan was unhappy with the marriage and truce, as he realized in would result in the expansion of the English settlement, he grew tired of the fighting and felt powerless to stop it.

Despite the truce, Jamestown remained a dismal place for most of the settlers. Food shortages and disease were rampant in Jamestown. Because Rolfe's tobacco crop showed such promise for profit, many settlers began growing their own, though few reserved space for corn. Tobacco became the cash crop of the Jamestown settlement. In 1614, conditions improved for settlers when Thomas Dale, using his powers as governor, began transferring some of the land to private ownership. In order to continue growing tobacco, the Virginia Company needed a substantial workforce. Through "the Headright System", English settlers were guaranteed 50 acres of land in return for three years of labor. "Heads of Families" who came to the New World were guaranteed 50 acres of land for each person they brought over. With their own lands, settlers began to build houses, tend to their land and grow crops which resulted in a new hope and inspiration for a successful colony.

Unfortunately, Jamestown's future was not bright. Powhatan's successor, Opechancanough, attacked the white settlements near Jamestown in order to prevent the settlers from taking more land for tobacco. It was a surprise attack, as the warriors approached the settlements as if they were preparing to trade. The attacks decimated the settlements and resulted in the deaths of 347 settlers, including John Rolfe. The attacks were especially surprising considering the peaceful relations that had reigned for many years. Although the Indians were driven back and eventually completely defeated, In 1624, as a result of the high mortality rates at Jamestown, and the colony's poor financial state, King James revoked the colony's charter and made Virginia a possession of the crown.