However, Telstra said in a financial filing of its own [pdf] that while the Tesla role would begin on November 13, Denholm would have to continue in the CFO and head of strategy role at the telco until May 6, 2019.
Tesla said Denholm will be serving as Chair on a full-time basis and that she will temporarily step down as Chair of the company's audit committee until she leaves Telstra.
The settlement requires Tesla to install an independent chairman, among other penalties.
The US Securities and Exchange Commission had charged Musk with securities fraud, alleging that he misled investors when he tweeted on August 7 that he had "funding secured" to privatize the electric automaker at $420 a share, a substantial premium over its share price at the time.More news: Red Star upsets Liverpool in Champions League
The move scotches reports that James Murdoch might have been appointed to the job. Tesla's shares soared following his comments.
The SEC accused him of manipulating the market and sued him in late September for making "false and misleading" statements to investors.
Musk had to step aside as chairman for three years and was also fined, but was able to remain Tesla's CEO.
"I look forward to helping Elon and the Tesla team achieve sustainable profitability and drive long-term shareholder value", she said in the statement.More news: Britons would back 'remain' in new Brexit vote: Channel 4 poll
But Tesla's stock had tumbled by more than 25 per cent before recovering the $7billion loss the SEC lawsuit incurred. However, the carmaker made what Mr Musk called an "historic" profit in the most recent quarter.
"So that she will be able to devote her full attention to the Tesla chair role, Robyn will be leaving her role as CFO and head of strategy at Telstra. once her six-month notice period with Telstra is complete", the carmaker said.
A Tesla spokesman said Ms Denholm would receive an annual cash retainer of $300,000, with $8000 in stock options annually.
Before moving to Telstra, she worked for Silicon Valley firms Sun Microsystems and Juniper Networks as well as consultants Arthur Anderson and Toyota.More news: Burley doubts over Lukaku getting back into Man Utd XI