Provisional governor

When Minnesota was admitted to the union in 1858, Sioux Falls became part of the newly forming Dakota Territory. Though Dakota Territory did not officially form until 1861, an interim provisional government formed in January 1859 and elected Brookings to the upper house of the interim territorial legislature. That legislative body later appointed Brookings Governor of Dakota Territory. However, the federal government refused to acknowledge either the provisional government or its territorial governor (his term lasted until March 2, 1861) as official. When the region finally did become an organized territory in 1861, Brookings was elected to the Territory Council for two years and later served three straight terms as a representative from Yankton County. In 1864 he served as territory speaker of the house and was appointed superintendent of the U.S. Military Wagon Road from Minnesota to Montana in 1865.

Later political career

After the assassination of Abraham Lincoln, territory Republicans opposing Lincoln's Democratic successor Andrew Johnson nominated Brookings as their congressional delegate, on an anti-Johnson platform. Brookings lost to fellow Republican Walter A. Burleigh.

Brookings served on the Territorial Council from 1867 to 1869, including a stint as council president in 1868. He also served as district attorney for Yankton County from 1867 to 1868. In 1869 President Ulysses S. Grant appointed him associate justice of the Supreme Court of the Dakota Territory. Brookings served in this capacity through 1873. Between 1883 and 1885 he worked as a member of South Dakota's constitutional convention.

On July 3, 1871, Brookings County was formally organized and named after him. The city of Brookings, South Dakota was also named for him, though he only ever visited the town twice. In 1871 Brookings helped organize the Dakota Southern Railroad, and spent the next ten years serving as an executive for the railroads that would eventually become part of Chicago, Milwaukee, St. Paul and Pacific Railroad. Brookings was among the first to ride a locomotive into Dakota Territory when the first Dakota Southern train entered the region on October 1, 1872.

Later life and death

In January 1885, Brookings bought and became editor of the Sioux Falls Leader newspaper (which later merged with the Sioux Falls Argus and became known as the Argus Leader). Brookings also served as president of the Minnehaha Trust Company, Director of the Sioux Falls National Bank, National Realty Company, and Safe Deposit Company.

Brookings died riding a streetcar in Boston, Massachusetts, on June 13, 1905, while on a return trip from visiting his hometown in Woolwich, Maine. He is buried in Yankton, South Dakota.