The Montana State Highway Commission was created in 1913 by the state Legislative Assembly. The original Commission was composed of three members. In 1917 new legislation altered the organization of the Commission by authorizing the appointment of twelve members according to geographic highway districts. Membership was changed again in 1921 to three members appointed by the Governor and in 1941 to five members, also appointed by the Governor. In 1971 the Commission was renamed the Montana Department of Highways, created by Chapter 7 of the Executive Reorganization Act of 1971 and implemented by executive order of the Governor on December 16, 1971. The Department of Highways took over all but the advisory functions of the State Highway Commission.

By 1972, the Department consisted of seven divisions: the Legal Division, Personnel Division, Centralized Services Division, Engineering Division, Motor Pool Division, Gross Vehicle Weight Division, and the Maintenance Division. Each division was headed by an administrator. The Centralized Services Division, Engineering Division, Motor Pool Division, Gross Vehicle Weight Division, and the Maintenance Division were furthered sub-divided into bureaus, headed by Chiefs. In 1991, the Department of Highways became the Department of Transportation.

At present, the Right-of-Way Bureau is under the umbrella of the Preconstruction Program, which administers the Highways Bureau, Bridge Bureau, Consultant Design Bureau, Traffic and Safety Bureau, Environmental Services Bureau, and the Engineering Information Management Section. Both historically and currently, it has been the Right-of-Way Bureau’s primary function to acquire land for highways, and deal legally with previous acquisitions of land. It also provides assistance and payments to individuals and businesses relocated by highways, designs the right-of-way, and arranges for relocating utilities that conflict with highway construction.