The Town Government consists of five Commissioners, elected at large by the voters of Poolesville for staggered four year terms. The Commissioners then elect one of their own as the President (informally known as The Mayor) and a Vice President. The Commissioners are responsible for setting policy through legislation, exercising executive functions and providing guidance to the Town Manager who handles the day-to-day operations of the Town through a Parks and Streets Department, a Water and Sewer Department, a Wastewater Treatment Department and a Town Clerk/Treasurer. The Town also has an Attorney, Engineer and an Accountant under contract. These individuals are tasked by the Commissioners through the Town Manager.

The Commissioners are assisted in governing the Town by six appointed Boards and Commissions. These include: the Planning Commission which exercises planning and zoning powers as outlined by the State of Maryland; the Parks Board which is responsible for advising the Commissioners on Park use, capital projects and future park sites; a Board of Elections who insures that local elections are held in accordance with local and state laws; a Sign Review Board whose responsibilities include approving all signs posted for use in the Town; a Board of Zoning Appeals which hears testimony and rules on various zoning issues; and an Ethics Commission who's responsibilities include ruling on conflict of interest issues.

The Town provides it's own wastewater treatment facility. It also provides parks, street lighting, roads repair and maintenance and trash collection. Poolesville levies its own taxes and fees, and has full planning and zoning authority. The Montgomery County Police Department supports the Town and has set up a Police Sub-Station at Town Hall. Animal control is also handled by the County.

The Commissioners meet twice a month normally on the first and third Mondays. The Parks Board normally meets once a month on the Wednesday after the first Commissioner meeting, and the Planning Commission normally meets on the second Wednesday following the first Commissioner meeting. The other Boards and Commissions meet on an as needed bases.