In 1964, he ran for Congress as a Republican in the 2nd District, which was anchored by Montgomery and included most of the southeastern portion of the state. He defeated 13-term incumbent Democrat George M. Grant by a shocking 25-point margin. Almost none of the district's living residents had been represented by a Republican before, and Dickinson was the first Republican to challenge Grant. However, as was the case in most of Alabama, most of the 2nd District's voters turned against the Democrats when U.S. President Lyndon B. Johnson signed the Civil Rights Act of 1964. Dickinson was also the beneficiary of long coattails from Barry Goldwater, who carried many of the counties in the district by staggering margins. Joining Dickinson in victory in four other House races were Jack Edwards in the 1st District, John Hall Buchanan, Jr. in the 6th District, Glenn Andrews in the 4th District and James D. Martin in the 7th District. That gave the Republicans, who had not elected anyone to the House from Alabama since 1901, a majority of the state's House delegation for the first time since Reconstruction. Dickinson was reelected by 9% in 1966, when Democratic gubernatorial nominee Lurleen Burns Wallace led her party's slate to statewide victory by easily defeating Martin. Dickinson was then reelected 12 times without substantive opposition. Dickinson was an important figure in shaping national defense policies during the 1970s and 1980s. As he gained seniority, he became ranking member of the House Armed Services Committee; and was a leading member of his party's conservative wing. He never served in the majority during his entire 28-year House tenure. However, he became very popular in his district, gaining a reputation for strong constituent service. Still, Democrats continued to hold most of the district's seats in the state legislature and would continue to do so well into the 1990s. In 1965, he made two speeches to Congress claiming that civil rights marchers were engaged in alcohol abuse, bribery, and widespread sexual debauchery at the marches: "Drunkenness and sex orgies were the order of the day in Selma, on the road to Montgomery, and in Montgomery." Dickinson concluded that it was part of a vast communist conspiracy: "... years ago a systematic plan was started by the Communists to divide the Deep South from the rest of the Nation by the very tactics they are now using" and characterized the participants as only posturing with a "facade of righteousness, smugness and respectability erroneously attributed to them, which allowed them to invade my home town and my State like a swarm of rats leaving an overturned hayrick." After Dickinson's April 27, 1965 speech, which included several sworn affidavits, Congressmen William Fitts Ryan and Joseph Yale Resnick rose in a blistering defense of the march and Dr. King. Ryan noted the deliberate attempt to smear the marchers: "I am sure that the gentleman from Alabama remembered the old legal adage: When you do not have the facts on your side, try the opposition." Resnick read testimonials from religious leaders present at the marches, all of whom denied the allegations laid by Dickinson. Religious leaders present at the marches denied the charges, and local and national journalists were unable to substantiate his accounts. Attorney GeneralNicholas Katzenbach stated that "Communists' have been remarkably unsuccessful in influencing any decisions and certainly have not capture any of the leadership ." The allegations of segregation supporters were collected in Robert M. Mikell's pro-segregationist book Selma. In 1990, Dickinson was re-elected by only 2.5% over state welfare commissioner Faye Baggiano, his first competitive contest since his initial run in 1964. The closeness of the race prompted Dickinson to decide against running for a 15th term in the 1992 elections, even though redistricting made the district safer for him on paper by shifting most of his black constituents to the 7th District. He is the longest-serving Republican congressman in Alabama's history.