In summer, 1815 he commanded the Army troops providing security for the large meeting of Native Americans and U.S. officials as they negotiated the Treaties of Portage des Sioux.

Using his political connections, John Miller was able to secure an appointment as Registrar of the Howard County United States General Land Office in Franklin, Missouri in 1818.

Miller held the Registrar's position until 1825, becoming friends with a group of men who would eventually be known as the "Central Clique" and dominate Missouri Democratic politics through the 1840s.

The governorship then fell temporarily to Senate President Pro Tempore Abraham J. Williams until a special election could be held on December 8, 1825.

[8] In that special election John Miller edged out Judge David Todd, William C. Carr, and Rufus Easton with 2,380 of the 4,933 votes cast.

After several days of searching the banks of the Mississippi River, Miller, General Edmund P. Gaines (Commander of the Western Department of the Army), Brig.

General Henry Atkinson (commanding officer of the sixth infantry regiment), and explorer William Clark selected a site near the city of "Vide Poche" or Carondelet, ten miles (16 km) south of St. Louis.

In July 1829 Chief Big Neck led a large group of Iowa Indians into their former hunting grounds in northern Missouri near present-day Kirksville.

At Miller's urging, the General Assembly petitioned the federal government to provide U.S. Army escorts to wagon trains as protection from Native Americans and bandits.

[14] In his final term Governor Miller recommended that a state bank be established, backed by the good faith and credit of the government.

This was in keeping with his belief in a hard money policy prevalent among Jacksonian Democrats and strong dislike of the Second Bank of the United States.

[1] Miller seldom, if ever, "made waves" in his six years in Congress, preferring to be a good "party man" and supporting the Democratic policies.

[7] Dismayed by the increasing acrimony in national politics brought on by sectional hostilities, Miller chose not to seek a fourth congressional term in 1842.