As long as these qualifications are met, then there should be no reason why one individual couldn't run for the highest office in the land. In the 2008 Democratic primary race, then-Senator Hillary Clinton of New York touted her experience (which is real, genuine, and legit), verse then-Senator Barack Obama of Illinois' lack of experience (which was just at the federal level of politics...or just ageism). Experience was the theme of the Hillary Clinton campaign in the first half of the primary before evolving to an experienced politician for the working class American.
Senator Clinton's experience then in 2008, qualified her to be president. Her resume included a college graduate, law school graduate, First Lady of Arkansas, First Lady of the United States and senator from New York, and now she can include Secretary of State, an old stepping stone to the presidency. Let's just say, she's gone up in value since '08.
In that primary race her argument that then-Senator Obama wasn't experienced enough never stuck and the reason is because he met the qualifications to hold the office just as men before him with a small policial resume, like Abraham Lincoln, Theodore Roosevelt, and John F. Kennedy.
While experience is not a qualifier to be POTUS, then-Senator Clinton's resume probably came the closest to having the chops for the job without having been president. She was married to the president so she has some first hand experience seeing what the office holder must go through. There has only been one person ready for the job of the presidency before winning on election day and that's Grover Cleveland...only because he had been elected president 8 years before resuming the office.
In 1992, then-Governor Bill Clinton of Arkansas just had five terms as governor under his electoral belt before running. His main opponent, President George H. W. Bush had an even bigger resume plus as the commander-in-chief during a time of war. In 1996, Senator Bob Dole of Kansas had racked up years of political service in Congress and even as a vice-presidential candidate on a national ticket. In 2000, Vice President Al Gore's resume led him to the nomination as the sitting v-p, just like Bush, while his opponent, Bush's son George W. Bush, got the electoral weight from one full term as governor of a large state, Texas, and an election to a second term. John Kerry used his military service in Vietnam and political service in the senate as building blocks to his candidacy and then-President Bush 43 used his first term on top of all his experience for reelection. So really there is no clear cut mold for a person to fit to become a nominee. Obama used his brief federal experience, and State-level experience, and everything that made him unique to help him win the nomination, just as his opponent Senator John McCain used to prove to the electorate that he too was qualified to be president. In 2012, Obama is using his first term and Mitt Romney (assuming he is the nominee) will use his one term as governor and business career (he'd be using his political career had he won the senator race against Ted Kennedy in 1994) to be president. So why in 2008, didn't Sarah Palin's unique resume make her qualified for the bottom of the ticket?
Her lack of intellectual curiosity was made clear in her interview with Katie Couric and then later with Charlie Gibson and it was nobody's fault but her own...and probably the McCain camp's vetting team. Palin's resume is a political dream come true and only if she had intelligence to back up her short political resume, she would be a political super-star just like Obama, Reagan, Bush 43 (pre-2006), and both Clintons. She can muster a following, but if there was only substance to back it up would her following become more powerful in putting her into a position of power.
There are only 3 qualifications to be POTUS and they are clearly stated in the Constitution. Individuals like Obama and Palin have vied for it and have had to prove themselves beyond the qualifiers mentioned in one of our founding documents. You don't have to be a life long politician to be president but you have to show some knowledge of current events...just like students in a social studies class. Or if you're lucky, you can run for a non-consecutive term like Cleveland...but that's difficult in this 22nd Amendent era we live in.