Born and raised in Boise, Idaho, Church was the younger of the two sons of Frank (II) and Laura Bilderback Church. His father co-owned a sporting goods store and took the sons on fishing, hunting, and hiking outings in the Idaho mountains. The family was Catholic and conservative, and Frank III attended St. Joseph's School as a youngster, where he went by the nickname "Frosty." His older brother Richard became a career officer in the U.S. Marines Corps, and retired as a colonel.

Church became an active Democrat in Idaho and after an unsuccessful try for the state legislature in 1952, he ran for the U.S. Senate in 1956. After a closely contested primary election against former Senator Glen H. Taylor, Church handily defeated Republican incumbent Herman Welker in the general election. At the age of 32, Church became the fifth youngest member ever to sit in the U.S. Senate. Church was reelected three times (1962, 1968 and 1974), the only Democrat ever to win reelection to the U.S. Senate from Idaho.  Upon entering the Senate in January 1957, Church made the mistake of voting on a measure against the wishes of Democratic Majority Leader, Lyndon Johnson, and Johnson punished Church by all but ignoring him for the next six months. Church found solace from Republican Minority Leader, William Knowland. However, Church managed to find his way into Johnson's good graces by providing key assistance in getting the Civil Rights Act of 1957 passed. LBJ was so grateful he made the young Idahoan a veritable protege, rewarding him with plum assignments, such as a seat on the prestigious Senate Foreign Relations Committee, a position which allowed Church to follow in the footsteps of his idol, William Borah. Recently declassified documents show that the young veteran also challenged his mentor, behind closed doors, after the 1964 Gulf of Tonkin incident, making this prescient warning: "In a democracy you cannot expect the people, whose sons are being killed and who will be killed, to exercise their judgment if the truth is concealed from them."  In 1967, a recall campaign was waged against Church by Ron Rankin, a Republican county commissioner in Kootenai County in northern Idaho. Rankin unsuccessfully sued Idaho's secretary of state to accept recall petitions. The U.S. District Court for Idaho ruled that the state's recall laws did not apply to U.S. senators and that such a recall would violate the U.S. Constitution. Allan Shepard, Idaho's attorney general at the time, agreed with the court's decision.  "It must be pointed out that a United States senator is not a state officer but a federal officer whose position is created by Article I, Section I of the United States Constitution," Shepard wrote in a June 17, 1967, opinion for the secretary of state. "There seems to be no provision for canvassing the votes of a recall election of a United States senator." Most commentators at the time believed that the recall attempt strengthened Church politically by allowing him to play the role of political martyr and he was reelected in the next year's election over Republican Congressman George V. Hansen 60% to 40%.

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