Using Wednesday’s price, Mr. Musk would need to satisfy the banks with more collateral if Tesla shares were to fall 43% to around $504. In that case, the banks would require a rebalancing that would call for an additional $14 billion, or 28.5 million shares at that level. That’s on top of the 70.9 million shares needed at Wednesday’s price for the original collateral.

Similarly, Tesla has long capped the amount Mr. Musk is allowed to borrow against his shares at 25% of the total value of the pledged stock. This suggests that if the deal used Wednesday’s share price, he’d need to pony up more if those shares fell more than 20% to below $705 and Tesla enforces its policy. These arrangements mean that in certain scenarios, he could be pressured to sell Tesla shares.

Tesla didn’t respond to a request for comment.

Mr. Musk sold roughly $4 billion worth of Tesla stock in the two days after agreeing to buy Twitter, selling a total of more than 4.4 million shares on Tuesday and Wednesday at prices ranging from around $870 and $1,000 a share, according to regulatory filings made public late Thursday.

The overarching story of Tesla’s stock has been one of growth, rising more than 18,000% since going public in 2010. But, like Tuesday, when it fell 12% as investors digested, among other things, what Mr. Musk’s involvement in Twitter might mean for other parts of his empire, the stock has been highly volatile. The Tesla shares are down more 20% since April 4 after he balked at joining the Twitter board, setting him on a path to bidding for the company.

Since 2010, positive and negative stock swings of 5% or more in a single day have totaled 318, according to FactSet data, including Tuesday when Tesla fell to $876.42 a share. In that same period,

Apple

has seen 57 similar days while

General Motors Co.

had 90.

At the end of 2021, Mr. Musk had 173 million Tesla shares, not counting his options. About half of his stake was already promised as collateral for personal loans, according to the most recent public record last year. Pledging doesn’t necessarily indicate that actual borrowing against those shares has occurred, the filing said. The most recent public filing in late 2020 said Mr. Musk personally owed a combined $515 million to

Morgan Stanley,

Goldman Sachs

and

Bank of America.

The business tycoon has long built his personal financial house on a complicated web of loans backed by his ownership stakes in the companies he backed, including his privately held rocket company, Space Exploration Technologies Corp.

Tesla has previously warned investors of the risk that a stock sale by Mr. Musk to cover loans could cause share prices to fall.

“If the price of our common stock were to decline substantially and Mr. Musk were unable to avoid a sale of the pledged shares (for example, by contributing additional collateral or reducing his leverage), Mr. Musk may be forced by one or more of the banking institutions to sell shares of our common stock,” the company wrote in a 2020 regulatory filing.

Along with competing for his attention, Tesla and SpaceX have over the years shared employees and resources—the Model S sedan prototype was developed under a tent inside SpaceX’s Hawthorne, Calif., headquarters.

In 2016, Mr. Musk led Tesla’s controversial acquisition of a struggling solar panel company called SolarCity Corp., where he was chairman and the largest individual shareholder. Opponents of the deal described it as a bailout for Mr. Musk, while he said it would fuel natural synergies. A Delaware judge ruled Wednesday that the deal was lawful.

Mr. Musk’s unusual finances are in part a legacy of the struggles Tesla and SpaceX faced during the Great Recession in 2008. He plowed what was left of his fortune from his involvement in

PayPal

into those ventures and was reluctant to sell his ownership stakes later as those businesses improved.

That history had left him a cash-poor billionaire for much of his career even while the Bloomberg Billionaires Index ranks him as the world’s richest man with a fortune of more than $250 billion.

To fund his life and investments, Mr. Musk has borrowed money against his shares in Tesla and SpaceX to avoid having to sell them, a common practice among some of the wealthiest Americans. Before Mr. Musk began selling billions of dollars of shares late last year to help cover taxes on his options that vested, the company reported in June that about half of the Tesla shares he held were being used as collateral for personal borrowing.

His finances have benefited by the fact that the valuations of Tesla and SpaceX have continued to grow, allowing him to borrow more with fewer shares down.

But Tesla shares have fallen precipitously on occasion, often triggered by events or predictions tied to the company’s prospects for growth.

Shares fell 21% on Sept. 8, 2020, after Tesla failed to be included in the S&P 500 as expected. Later that autumn they rose 8.2% the day after it was announced that the company would be included in the benchmark gauge of U.S. equities.

In early 2019, a dark cloud descended over Tesla as shares fell 43% in May from the year’s start among concerns about the company’s outlook. Mr. Musk was struggling to export the Model 3 compact car to China and Europe and with efforts to lower the vehicle’s price in the U.S.

Once those challenges were addressed and Tesla opened its first China assembly plant, the stock would begin the run that took it to new heights as the world’s first auto maker valued at more than $1 trillion in 2021.

During those times when Tesla shares have fallen dramatically, attention often focuses on the margin call price for Mr. Musk’s shares.

In May 2019, for example, some short sellers—those investors who benefit from a decline in share price—were pushing a theory on what the trigger price would be for a selloff as Mr. Musk moved to cover his position.

That didn’t happen, but his family has clearly felt that pressure before. In 2015, Tesla board member and Mr. Musk’s younger brother,

Kimbal Musk,

faced a possible margin call on shares of SolarCity which had fallen to half their value from the start of the year, according to court records. Under financial pressure, he sought a loan from his brother.

“You know that I don’t actually have any cash, right?” Mr. Musk responded, according to records released in litigation dealing with the acquisition. “I have to borrow.”

Write to Tim Higgins at Tim.Higgins@WSJ.com