For an "unaffiliated" House candidate, the landscape is a little less harsh. Since nonbelievers tend to live in urban areas, it's conceivable that an openly atheist candidate could find a large enough base to support a primary or general election run against more religious competitors. Even still, given the relatively small number of unaffiliated, this isn't very likely.

The bright side is that partisanship would carry a lot of water for an open atheist or agnostic who made it through the primary. In a strongly Democratic or Republican area, the religious affiliation of the majority candidate doesn't really matter in a general election. The bigger obstacle would be the primary. This is probably less true in a statewide election, and not true at all in a presidential election. Particularly in states where the parties are evenly matched, the lack of religious belief could be enough to lose an election. And since party activists would know this, winning a primary—as a nonbeliever—would be much more difficult.

Is this a form of the "closet," as Andrew Sullivan describes? Perhaps. Non-belief is definitely an obstacle for an aspiring politician, and there really isn't any benefit in "coming out" as an atheist or agnostic. The United States is still too religious for that to be viable in anywhere but the most liberal enclaves, where non-belief is acceptable. Yes, the population of "unaffiliated" people is growing, but the strong cultural legacy of religious belief might keep that from translating into greater openness for less religious candidates. But we'll see.