Like his father, Boudinot was drawn to newspaper work, taking the editorship first of the Fayetteville Weekly Arkansian
and then of the Little Rock True Democrat
in 1860. Boudinot also became involved in Democratic and Confederate politics during this period, becoming chairman of the Democratic State Central Committee in 1860 and secretary of the Secession Convention the following year.
The Civil War again split the Cherokees into two warring factions, with battles fought throughout the tribal nation between Union and Confederate Cherokee forces. Boudinot served briefly with his uncle Stand Watie's Confederate regiment, achieving the rank of lieutenant colonel. In 1863 the southern faction of the Cherokees elected Boudinot as their delegate to the Confederate Congress at Richmond. At the war's end, Boudinot represented the southern Cherokee faction in the negotiation of the Cherokees' 1866 treaty with the United States.