Oldenbarnevelt, two years after William's assassination, in 1586 accepts the appointment by the States of Holland as the province's landsadvocaat, in which office he becomes the real trustee of William the Silent's political inheritance.

While the latter's son, Maurice of Nassau, a brilliant military commander, is in charge of the actual warfare in the field, it is Oldenbarnevelt who, at first in close collaboration with him, mobilizes and coordinates the country's available energy and resources, thus making warfare possible.His power comes not from his office but from his being the leader of the ruling oligarchy of Holland, the preponderant province.

Although theoretically a servant of only one out of seven sovereign provinces, Oldenbarnevelt, who himself undertakes diplomatic missions to France and England, is virtually the union's foreign secretary.