The resignations were abrupt and unexpected, two quick-fire blows to a separatist movement already suffering reversals on the battle field of eastern Ukraine.
Alexander Borodai, the premier of the self-proclaimed Donetsk People's Republic, and Igor Strelkov, his military commander, had together formed the rebels' leadership against Ukrainian troops since armed men first seized state buildings across eastern Ukraine in April. Friends from Moscow and comrades in arms, they were viewed by the separatists and by Kiev as Russia's men. Their successive departures in the past two weeks may mark a turning point in a conflict which has dragged ties between Russia and the West to their lowest since the Cold War.
Among separatist ranks, the news has fuelled fears that other Russian fighters may abandon the insurgency. Interviews with rebel fighters and recorded conversations of rebel leaders provided by Ukrainian security services reveal a separatist movement struggling for survival against larger and better-equipped Ukrainian forces.
Some rebels, speaking on condition of anonymity, see the command changes as an attempt by Moscow to distance itself from the conflict. The United States and European Union have accused Russia of training and arming the separatists and imposed economic sanctions on Moscow. One rebel source said the new leadership was meant to bring about a "de-escalation" of the conflict - a term used by the West in demanding Russia turn off financial and military support to the rebels. The Kremlin denies such involvement. Another rebel source said Borodai and Strelkov, whose real name is Igor Girkin, slipped into Russia last week under cover provided by armed separatists. Self-styled deputy prime minister Vladimir Antufeyev confirmed that Strelkov had left the region.
A recording of separatist leaders released by Ukraine's state security service suggested more Russian citizens fighting in Ukraine were looking to leave. A rebel fighter told Reuters the insurgency was in a critical phase. "Everything is coming to a head," he said.
Much about the circumstances of Borodai and Strelkov's departures is unknown, and it is difficult to tell yet whether they mark a change of tactics or a winding down of Russian support.
Rebel website Novorossiya reported 1,000 fighters, more than 100 armoured vehicles and new weapons supplies had been promised in return for Strelkov's resignation. It did not say which entity or individual had made this promise.
The rebel region's new prime minister Alexander Zakharchenko said in a video after Strelkov's resignation that 1,200 fighters trained in Russia and more than 100 military vehicles were joining the fight. He later denied making the comments.
Any sign that Russia is increasing its support of the rebels would cast doubt on Moscow's sincerity in saying it seeks a negotiated settlement to a crisis triggered earlier this year by the ousting of Ukraine's pro-Moscow president Viktor Yanukovich.
Strelkov made his name defending the stronghold of Slaviansk, downing Ukrainian aircraft and leading tactical manoeuvres. The loss of his experience is a setback for the separatists as the Ukrainian army gains ground along the border through which Kiev says Moscow has ferried weapons and fighters to rebels. Zakharchenko said Strelkov was simply going on a month-long vacation.
A rebel named Yevgeniy who served with Strelkov in Slaviansk, said the resignations of Strelkov and Borodai, long-time friends who worked together briefly in business in Moscow, came at a difficult moment. "In the context of these events it doesn't look very good. But there is no panic. These people have done a lot for us," he said by telephone. He said there were no plans to retreat or surrender. "I have no place to go."
Some in the rebel ranks suggest the leadership changes were an attempt to give a more local face to a conflict that had been led mostly by Russian nationals, fuelling discontent among Ukrainian fighters and strengthening Western assertions that Vladimir Putin was pulling the strings.
The United States and European Union introduced their latest round of sanctions against Moscow following the downing of a Malaysian airliner over rebel held territory in July. They say the aircraft was almost certainly brought down by pro-Russian rebels supplied with a Russian missile system.
The downing of the plane may prove to be the turning point in the conflict.
"I know the reaction of people who saw Putin at the moment when the information (about the Malaysian plane) was delivered to him. It was a reaction of absolute shock," rebel commander Alexander Khodakovsky, leader of the rebel Vostok Battalion, told Reuters last month. Hours after the crash, Putin expressed his condolences but also suggested Ukrainian President Petro Poroshenko bore responsibility for the fighting along the plane's flight path.
Changes in the rebel leadership come as Moscow appears to be dialling down its rhetoric.
Putin is due to meet with Ukraine's Poroshenko on August 26, along with the European Union and Kazakhstan and Belarus. The Russian president's most recent speech in Crimea, the Ukrainian region annexed by Moscow, was conciliatory in tone. Unusually for a Putin set-piece speech - it was not broadcast live on state television and news bulletins only made brief mentions.
'A War To Win'
Those at the top of the insurgency said the reshuffle aimed to combine a political and military leader in one role - in Zakharchenko who replaced Borodai as premier last week.
"In every other democratic country in the world, the political head is always the commander in chief. That's what we have here," said Zakharchenko's right hand man Andrei Purgin, who originally conceived the Donetsk People's Republic as a social movement in 2005. Zakharchenko, a blonde-haired and barrel-chested native of Donetsk region, made a name for himself leading rebels units against Ukrainian troops. "We have to win a war and today there is no better candidate than Zakharchenko. This is a person who will mobilise the people of DNR for the front. And he is just as much prime minister as he is chief commanding officer," said Purgin.
Strelkov's replacement is a little known rebel officer, who hails from the neighbouring region of Luhansk, named Vladimir Kononov who goes by the nom de guerre of Tsar.
'A Month Left'
Morale is still high in separatist ranks, said Purgin. Separatist websites claim tactical victories for the rebels including the take over of a border crossing point east of Donetsk at Marynivka and the attack on a military brigade from Lviv in western Ukraine.
But Russian military analysts say Ukrainians, with their greater firepower and higher numbers, have the advantage. A recording released by Ukraine's security services, purportedly of a Russian fighter speaking with an officer from Moscow's Federal Security Services (FSB), pointed to rifts between fighters from Russia and local rebels and said DNR had little time left.
The fighter, "Trifon", who fought alongside Strelkov in Slaviansk uses Russian curses to condemn local rebels for doing "nothing at all" and says he needs a way out of the region to return to Russia. "I think DNR has a month minimum," he says in the recording which Reuters was unable to verify independently.
Many locals still pledge allegiance to the separatist project but even among the few who have stayed behind in the stronghold of Donetsk, some are making their frustrations with the separatists known.
After the first shelling in the centre of the city last week, a middle aged man accused the rebels of launching the attack that killed at least one person in the centre of the city. In return, rebels pulled him to the ground demanding he ask for forgiveness on his knees.
Another woman across the street pointed to the separatists saying: "They're the ones who did this, it's members of the DNR themselves."