The tensions over Downing's focus on Gates' marital infidelity came after rounds of questioning where the temperature was somewhat cooler than what it had been on Tuesday afternoon, when Downing drubbed Manafort's ex-business deputy about his admission that he embezzled from his former boss, and other alleged criminal activity.
Mr Downing forced Gates to admit he had stolen hundreds of thousands of dollars from Manafort by filing bogus personal expenses claims and that he had engaged in an extramarital affair and kept an apartment in London for that objective.
"After all the lies you've told, and the fraud you've committed, you expect the jury will believe you?" The charges are not related to Manafort's work with the Trump campaign.
Gates struggled so badly to give a straight answer that eventually Judge T S Ellis III was forced to intervene. He spoke in federal court in Virginia when Manafort pleaded not guilty to bank and tax fraud charges there, and defense attorneys accused him of leaking information to the press on Manafort before joining the special counsel's office. He also admitted to embezzling money from other employers in the past.
For most of his testimony, Gates did not look at Mr Manafort, while the defendant stared intently at his former partner.
Asked if he got any personal benefit from Mr Manafort's falsified loan applications, Gates responded: "No, I did not". Gates testified they were not loans but compensation to Manafort. He is expected to face a bruising cross-examination as defense lawyers try to undercut his credibility and pin the blame on him.
Manafort and Gates were the first two people indicted in Mueller's investigation into potential ties between Russian Federation and the Trump campaign.
Gates said that even while he was committing crimes with his boss he was stealing from him, creating false bills to siphon off hundreds of thousands of dollars from the Cyprus accounts.
In 2015 and 2016, Gates said, Manafort "requested a team of people to pull together" documents to apply for bank loans in order to keep pace with payments to maintain his luxurious lifestyle. Gates also provided the first witness testimony that overlaps with Donald Trump's presidential campaign.
Gates also testified on Tuesday how he and Manafort hid income earned for political work in Ukraine, explaining their efforts to set up companies in Cyprus so they could easily be paid by Ukranian businessman who held bank accounts there.
Although the allegations of collusion between Donald Trump and Russian Federation are not at issue in this trial, any significant blows to the government's case are likely be seized on by the president's defenders, including conservative media, to support his contention that Mueller's investigation is a "rigged witch-hunt".
After Gates described his theft as "unauthorized transactions" instead of embezzlement, Downing prodded him to use the latter term - and Gates ultimately relented, saying, "It was embezzlement from Mr. Manafort".
Jurors saw emails from Manafort imploring Gates to help a banker, Stephen Calk, make inroads into the campaign, inauguration and administration.
Downing wondered aloud why Gates had shown "perfect recollection" during examination by the government but was now much less precise under cross-examination by Manafort's defence. Gates testified that Manafort asked him to float Calk, who was on Trump's economic advisory council, for Secretary of the Army.
Downing's question came after prosecutor Greg Andres had stressed in his questioning of Gates Wednesday morning that his plea deal would be ripped up if he lied from the stand. The firm's director was known to Manafort and Gates as "Doctor K".
However, when Andres returned to the podium for another chance to question Gates, Gates said that Manafort did reach out to a Ukrainian businessman before his Federal Bureau of Investigation interview to get more information about the entity that the businessman used to pay him and to make sure that it was "clean", meaning it was only used to pay Manafort.