John Lamont, who as party chief whip is Davidson's "eyes and ears", is to stand in the party's first "open primary" selection contest for Westminster.
But a senior Tory source said Lamont's potential departure was a blow for the leader.
Davidson secured the Tory leadership in 2011 in spite of an overwhelming majority of her own MSPs voting against her. Of 15 Tory MSPs, only two - Lamont and John Scott - came out in favour of her candidacy.
Lamont, the MSP for Ettrick, Roxburgh and Berwickshire, was rewarded with the job of chief whip. But Lamont sees his future as the MP for Berwickshire, Roxburgh and Selkirk (BRS), a seat held by LibDem incumbent Michael Moore.
The Tories opened up their candidate selection system to allow anyone on the electoral register in the Borders seat a vote in the contest.
The selection, which takes place in Kelso today, is seen as a pilot that could be rolled out to other seats.
Hundreds are expected to vote for either Lamont or his rival, party councillor Michelle Ballantyne.
Rules have allowed each candidate to spend only £200 in the contest and Lamont has been energetic in contacting local Conservatives.
In one letter, a copy of which the Sunday Herald has obtained, Lamont does not mention that he is an MSP: "As a son of a local farmer, I understand the need to provide a strong voice for unique rural communities like those in the Borders."
Lamont's decision is controversial as a victory at tomorrow's selection and at the 2015 General Election would mean he becomes an MP and MSP for around 12 months, a practice dubbed 'double jobbing'..
As Davidson's most trusted ally in the Tory group, Lamont's departure could also leave her exposed. MSPs remain sceptical about Davidson.
A Tory source said: "This is a double-edge sword for Ruth. She wants to win the seat, but John was one of only two MSPs to support her leadership bid. Her number of allies will be cut in half."
Ballantyne said: "John has written to every man and his dog. I've been more focused and emailed lots of people. My campaign has also been based on word of mouth."
She added: "I suppose the question is, 'what's wrong with being an MSP? Is it not adequate?'."
SNP MSP for South Scotland Joan McAlpine said: "Given past Tory criticism of the First Minister for serving out what was a transitional dual mandate it is the height of hypocrisy for the Tories to seek new and wholly unnecessary dual mandates. But it does show that their priorities lie in London, rather than the Scottish Parliament."
A Scots Tory spokesman said: "If successful in both the open primary and subsequent General Election, John will stand down from Holyrood at the next electoral opportunity.
"This is in line with Scottish Conservative policy."
Lamont could not be reached.