By the 1670s, Dirck Wesselse had entered public life - serving as an Albany constable, overseer, and juror. He was entrusted with a share of the community registry - acting as a clerk and notary. This successful businessman also was a frequent petitioner and plaintiff before an Albany court that was called on to decide on an expanding range of issues. In 1676, he was appointed one of the court magistrates. Over the next three decades Dirck Wesselse would hold almost every elective and appointive office on the local level. Official records show him to be among each body's most consistent members.
During the mid-1670s, his budding career received an added boost from an association with newcomer Robert Livingston - who shared some of his clerical and business opportunities with this willing and able Albany insider. Livingston included him in a number of land petitions that provided Dirck Wesselse with substantial acreage in the upriver region of New York.
By the 1680s, Dirck Wesselse had emerged as one of the foremost Albany leaders. In 1683, he was chosen to represent Albany County in a provincial assembly called by Governor Thomas Dongan. Although that body was short-lived, in 1686, he was appointed an alderman under the new city charter. Shortly thereafter, he was called on to replace Isaac Swinton as recorder or deputy mayor. He served as recorder until 1696, when he was appointed mayor of Albany.
Dirck Wesselse stood with other established Albanians to resist the self-imposed leadership of Jacob Leisler during the politically uncertain years of 1689 to 1691. With mayor Pieter Schuyler pre-occupied with military matters, deputy mayor Wesselse held fast to Albany's charter against the claims of Leisler's lieutenant who claimed that it and all enactments of the now-deposed James II were illegal and void.
Over the next half decade, Dirck Wesselse served in the Albany municipal government as recorder, justice, and Indian Commissioner, and, from 1696 to 1698, as mayor of Albany. In 1691, he was chosen to represent Albany County in the provincial Assembly - which was reinstituted after New York became a royal province. He was re-elected annually and served until 1696. Following a four-year break, in 1701, Dirck Wesselse again was elected to the Assembly. But this time he was disqualified and refused admittance because he no longer resided in Albany. Although he still maintained a substantial home and held other property in the city, by that time he had relocated to his country estate on the Roeloff Jansen Kil. Although his ouster was politically motivated, it ended the public career of the sixty-three-year-old pioneer. After 1701, Dirck Wesselse is best characterized as a country landholder.
During the 1690s, he had purchased 1800 acres on the Roeloff Jansen Kil from Robert Livingston. Livingston's willingness to share some of the best land in the heart of the Livingston estate with Dirck Wesselse testifiies to the closeness of their relationship. In 1695, Wesselse built a country home or bouwerie on the property. He continued to improve that property and, with his large family, retired there by the early decades of the eighteenth century. By that time, sons Wessel and then Johannes had reached maturity and could take over his more demanding Albany-based enterprises.
Calling himself "late of Albany, but now of the Manor of Livingston," Dirck Wesselse made his will early in 1715. It named his wife and eleven surviving children in detailing the disposition of his large and diffused estate. This city father died on his bouwerie on September 18, 1717 at the age of eighty.