He was elected in 1864 to the Thirty-ninth, and reelected to the Fortieth and Forty-first Congresses (March 4, 1865 – March 3, 1871). Cullom returned to the Illinois House from 1873 to 1874, serving again as Speaker. In 1876, he was elected Governor of Illinois, defeating Lewis Steward by 6,834 votes. He was re-elected in 1880, becoming the first Illinois governor to be re-elected after a four-year term. Under Cullom's governorship, the Southern Illinois Penitentiary was commissioned, the Great Railroad Strike of 1877 was quelled, the Illinois Appellate Court was founded, and the Illinois State Board of Health was established. He resigned in 1883 to take office as a US senator; Lieutenant Governor John Marshall Hamilton assumed the governorship in his place. Cullom was elected to the United States Senate in 1882, and reelected in 1888, 1894, 1900 and 1906, serving from March 4, 1883 to March 3, 1913.