The university considers June 24, 1918, to be its founding date; this was the first day of classes for the Dickinson Normal School.

In 2011, the university was discovered to have overstated its enrollments by practices such as counting people as students who had merely attended a conference on the campus.

[9][10][11] A North Dakota University System audit report released in February 2012 found that the school had relaxed standards and waived some requirements to increase enrollment of foreign students and had, over a period of several years, awarded degrees to 584 foreign students who had not completed the required coursework.

News media accounts described the audit report as depicting Dickinson State as a degree mill.

[13][14][15][16] The audit had been requested by the university's president, Douglas Coston, who took office as Interim President in August 2011, after some university international agreements were found not to conform with requirements of the North Dakota State Board of Higher Education and the Higher Learning Commission.

[17] Six months later, in July, Dickinson's regional accreditor, the Higher Learning Commission (HLC), placed the university "on notice," requiring the university provide detailed responses to concerns found in the accreditor's recent site visit.

[20] The following year, the university changed its academic policies to increase class sizes and require faculty to teach more students.

Dickinson State University students are encouraged to complete their general education requirements by the end of the sophomore year.

The men's track and field team won NAIA national championships three consecutive years from 2004 to 2006 under coach Pete Stanton.

On April 30, 2013, both chambers of the North Dakota Legislative Assembly passed a bill appropriating $12 million to Dickinson State University to award a grant to the Theodore Roosevelt Center for construction of a building to be named the Theodore Roosevelt Presidential Library.