She will be leading a team of 30, and replaces Anne Kendall, who stepped away from the role in July for personal reasons but is expected to return in an advisory role.
Cirkle chairman Caroline Kinsey praised Allchurch as "intelligent and warm" with an "incredibly strong work ethic".
She added: "Ruth has the perfect blend of experience to be joining Cirkle. Her understanding of consumer and b2b audiences, her knowledge of local and global campaigns and her insight into both agency and in-house roles make her uniquely placed to be leading the team."
In her role at Diageo Allchurch is responsible for leading the strategy on its core brands – Guinness, Tanqueray, Gordon’s, Pimm's, Smirnoff, Captain Morgan, Johnnie Walker and Classic Malt – across 14 countries.
Before her time in-house, which has also included handling trade PR strategy for Diageo, Allchurch worked for Cohn & Wolfe, Fishburn Hedges and Weber Shandwick.
Her replacement has not yet been announced.