But the two-term senator has quickly galloped back in the polls, demonstrating herself as a formidable challenger to Miller, who is struggling with a series of controversies.
Most recent polls show Murkowski trailing behind Miller by only 1 to 2 percentage points, within the margin of error.
Democratic candidate Scott McAdams is at a distant third, although his recent advertising campaign touting his Alaskan roots has boosted him in the polls since August, when even Democratic National Committee spokesman Brad Woodhouse couldn't recall his name.
Both Miller and Murkowski have stepped up their assaults, releasing powerful ads touting their own achievements while attacking each other.
"The horses are coming around the final bend right now and they're not in the absolute final sprint, but one of them's got to get a kick coming out of the bend and look strong in the next week, and whoever can create that momentum will be the one that draws some of that indecisive support onto them," said Alaska pollster Ivan Moore.
Miller has been dogged by a series of damaging revelations since he rode to victory on the back of the Tea Party Express and an endorsement from Sarah Palin.
First was the alleged feud between him and Todd Palin over Miller not wholeheartedly supporting Palin for president, when Miller was asked the question on a Fox News show.
Then there were Miller's comments questioning the constitutionality of federal health care benefits and suggesting that Social Security should be privatized and Medicare should be phased out. Opponents attacked those comments as hypocritical after reports emerged that Miller and his wife themselves received Medicaid.
Miller has also been under scrutiny by Alaskan media concerning his actions as an attorney at the Fairbanks North Star Borough. The liberal Alaska Dispatch published a report earlier this month alleging that Miller used the borough's equipment to oust Republican party chairman Randy Ruedrich.
On Monday, Miller admitted that he was disciplined for violating the borough's ethics policy in 2008 but denied any other wrongdoing.
"The event in question is something that happened on my time off. So it was during the lunch hour," Miller told CNN's John King. "I will tell you that anything that I've done that's not right, it's been accounted for and it's been taken care of and I move on and I learn from mistakes."
Miller denied -- counter to statements by his former boss -- that he was ever threatened with termination.
Alaska Senate Race a Toss-Up as Murkowski Rises in Polls
Miller charged that the blogger "invaded public space," was "assaultive" and apparently "shoved somebody," leading to his arrest.
But while Miller's lead in the polls has shrunk, Murkowski faces a challenging road ahead. Her name is not on the ballot -- as Miller points out in a new campaign ad inspired by the "Old Spice" man -- and she only has two more weeks to drive her "Get Out The Vote" campaign.
None of the three candidates who lodged write-in campaigns in Alaska were successful. No Alaskan candidate for statewide office has won more than 27 percent in a write-in campaign, and nationally, only one U.S. Senator in history has been elected via a write-in campaign, according to an analysis by the Smart Politics blog.
Additionally, Murkowski -- despite being a member of the Republican leadership -- was denounced by the establishment when she announced her write-in campaign. National Republicans, at least on the surface, have put their support behind Miller instead.
What Murkowski does have going in her favor is that she is virtually a household name. Her father was a state senator and governor until 2006 and she was a member of the U.S. House of Representatives before becoming a senator.
"Of course a write-in can win," Moore said. "It just needs a situation where the will is there amongst the people and the money is there to educate them about the fact that it's happening."
McAdams has mainly stayed out of the fray, running what Moore calls a rather "folksy campaign" that focuses on Alaskan issues. But McAdams is constrained by lack of notoriety and a small Democratic base in a state that is predominantly red.
Murkowski, Miller and McAdams have all seen a surge in their coffers since the Alaska Senate race grabbed the national spotlight.
McAdams reportedly raised $650,000 since the GOP primary. While Murkowski raised less in the same time period, she has more than $1 million in her campaign coffers. Miller raised more than both his chief opponents combined, reportedly totaling more than $1 million.