In 1847, during the Mexican–American War, he recruited a company for the 12th U.S. Volunteer Infantry and was commissioned a captain, serving under General Winfield Scott.

In November 1858, while Denver was still serving as territorial governor, William Larimer, Jr., a land speculator from Leavenworth, planted the townsite of "Denver City" along the South Platte River in Arapaho County in western Kansas Territory (the present-day state of Colorado).

Denver retired as territorial governor in November 1858, was reappointed Commissioner of Indian Affairs, and served until his resignation on March 31, 1859.

A few months after the start of the American Civil War in early 1861, President Abraham Lincoln commissioned Denver a brigadier general in the volunteer army on August 14.

[2] On May 27 General Sherman again selected Denver's brigade to be one of the leading units in an attack against the Double Log House.

Denver and Morgan L. Smith's brigade successfully stormed the log cabin turned block house.

During this engagement Major General Ulysses S. Grant was present on the battlefield and indicated his approval of the handsome manner in which the troops behaved.

[3] After the fall of Corinth Denver continued in command of his brigade, serving on garrison duty in Mississippi.

During the early stages of the Vicksburg Campaign Denver was in command of the 1st Division, XVI Corps, until his resignation from the Union Army on March 5, 1863.