On June 2, incumbent Larry Rhoden and Toby Doeden advanced to a Republican primary runoff on July 28. Neither received the 35% of the vote required to win the primary outright. As of June 3, Doeden received 31% of the vote, Rhoden 25%, Dusty Johnson 23%, and Jon Hansen 21%. This was the first time a gubernatorial primary went to a runoff since South Dakota passed a runoff law requiring 35% of the vote in 1985.

Rhoden was formerly lieutenant governor and replaced former Gov. Kristi Noem (R) on January 25, 2025, when Noem became the secretary of homeland security under Donald Trump (R). South Dakota Searchlight's editor-in-chief Seth Tupper said: "[P]eople are viewing this as an open seat. Kristi Noem resigned, and yes, the Lieutenant Governor came in and you could call him an incumbent, sort of, not really, but kind of. ... And I think a lot of people underestimated Governor Rhoden's ability to campaign for this seat. ... [B]ut I don't think it caused anybody to say, oh, I'm not going to run now, because open seats don't come along very often, obviously, in South Dakota Republican politics."

Rhoden is the governor of South Dakota. He said, "I want to keep South Dakota strong – strong families, strong businesses, and strong institutions. I want to keep South Dakota safe – with low crime and respect for law enforcement. And I want to keep South Dakota free – freedom will continue to be our calling card as long as I am governor."

Doeden is a car dealership and rental property owner. He said, "As governor, I will stop the reckless spending and fight back against crushing property taxes so everyone can own a home, and work with President Trump to round up illegal immigrants and get deadly drugs off our streets."

Hansen is the speaker of the South Dakota House of Representatives and a lawyer. He said, "As Governor, [I] will lower your property taxes, root out corruption, stop wasteful government spending, preserve the South Dakota way of life, and keep South Dakota free, safe, and sane."

Johnson represents South Dakota's At-Large Congressional District. He said, "It’s time for a new chapter—a chapter that drives South Dakota to a brighter future where we build better schools and safer communities, a chapter that governs with conservative principles to create new jobs, new businesses, and new opportunities in every community, and a chapter where being a workhorse, not a show horse, still means something."

In South Dakota, the gubernatorial nominee is selected in the primary. The gubernatorial nominee then chooses a lieutenant gubernatorial running mate, and they run together on a single ticket in the general election.