Under the leadership of the Oklahoma secretary of transportation and ODOT executive director, the department maintains public infrastructure that includes highways and state-owned railroads and administers programs for county roads, city streets, public transit, passenger rail, waterways and active transportation.

"[5] The predecessor agency to ODOT was the Department of Highways, which began operations in 1911, four years after Oklahoma statehood.

ODOT's annual budget of both federal and state funds is applied to highway construction and maintenance activities, railways, waterways, rural public transit programs and administration statewide.

The department maintains 139 miles (224 km) of state-owned railway, which are operated through leases with railroad companies, administers the Federal Highway Administration's Grade Crossing Safety Program which provides funding to make safety improvements to Oklahoma's nearly 3,800 at-grade public railway/road intersections, and manages the Amtrak Heartland Flyer passenger rail service in partnership with the Texas Department of Transportation.

It is the duty of the commission to establish agency policies, award contracts, approve budgets and conduct oversight.

[16] The Department of Transportation receives appropriations from the Oklahoma Legislature and direct streams of revenue authorized by State law.

The department's annual budget is primarily divided between two major areas: Operations and Capital Programs.