His chief assistant, and the second officer in rank, was the deputy. As the title suggests, he might be deputized to perform virtually any function of the governor, including that of presiding at courts in the governor's absence. But he also had important functions of his own. He is perhaps best described as the chief administrative officer of the company. He was specifically charged with superintendence over all lesser officers, and he had a primary responsibility for contracts and other business arrangements relating to the dispatch of shipping, provisions, and passengers to Virginia and to the receipt, storage, and marketing of cargoes returned from the colony. At all times, he acted, or was supposed to act, in accordance with instructions from the court, council, or treasurer, but all such instructions were necessarily general in character. Many were the opportunities to use his own judgment, or to confer a favor, as he handled business transactions involving hundreds or even thousands of pounds. For his assistance and perhaps to keep a watch on him, he had a committee of sixteen men chosen by the court under a provision requiring that a fourth of the number should be changed each year "to the end [that] many be trained up in the businesse." The committee may have been new, but the deputy's office was old. It had been occupied for many years before the spring election of 1619 by Alderman Johnson. Some of the more serious charges brought against Smith's administration related to the management of the magazine, as the stock of supplies periodically forwarded to the colony was generally described. Johnson had managed the successive magazines, each separately financed by its own joint-stock, until in 1619 he was replaced by John Ferrar.
The council, still described as His Majesty's Council for Virginia, had become a large and unwieldy body, with many of its members inactive. Its influence on the conduct of Virginia's affairs was now decidedly less important than in the earlier years. According to the Orders and Constitutions, no one "under the degree of a Lord or principall magistrate" was thereafter to be elected to the council except "such as by diligent attendance at the courts and service of Virginia for one year at least before, have approved their sufficiency and worth to the Companie." As this statement strongly suggests, a place on the council was for many members an honorary post through which one might lend the prestige of a great name to a worthy undertaking without assuming much real responsibility. Nevertheless, the legal powers of the council under the Virginia charters made its services indispensable, and made it desirable that at least a few of its members should be intimately acquainted with the business. The treasurer was supposed to consult with the council on important occasions, and especially on matters pertaining to the government of the colony. All formal instructions to officers in the colony had to be sent in the name of the council and over its seal. In any case of removal from office, in London or at Jamestown, the cause had to be considered in council before it could be taken before the adventurers. But any seven members made a quorum giving full power to actions taken in council, and the treasurer, who was always a member of the council, had the custody of its seal.