The two sides have gone to war twice, in 1990 and 2020, leaving tens of thousands dead, and clashes regularly erupt over the territory, an Armenian-majority region inside Azerbaijan.
Tensions have spiked again this week after Azerbaijan announced it had set up a checkpoint on the Lachin Corridor, the only land link between Armenia and Nagorno-Karabakh, sparking an angry response from Yerevan.
Armenia views the move as a violation of the cease-fire negotiated between the two sides.
On Sunday US Secretary of State Antony Blinken held a dinner with Armenian Foreign Minister Ararat Mirzoya and Azerbaijani Foreign Minister Jeyhun Bayramov.
The US diplomat then kicked off the expected four days of talks between the two sides Monday at a State Department facility outside Washington.
"The US is pleased to be hosting Foreign Minister Mirzoya of Armenia and Foreign Minister Bayramov of Azerbaijan to facilitate negotiations this week, as they work together to pursue a peaceful future for the South Caucasus region," said State Department spokesman Vedant Patel.
"The secretary believes that direct dialogue is key to resolving issues and reaching a lasting peace," Patel added.
Blinken also spoke Sunday with Azerbaijan President Ilham Aliyev, expressing concerns about the checkpoint, which he said "undermines efforts to establish confidence in the peace process," according to a State Department statement on their call.
"We have not parsed our words about the need for the free flow of traffic and people and commerce through the Lachin corridor," said Patel.
- Aiming to normalize relations -
Speaking on grounds of anonymity Monday, a US official said the talks aim more at "an agreement on normalization of relations" rather than a peace treaty.
"Our goal is to make sure the ministers can sit down and talk to each other," the official said.
The United States expects the two sides to have a forthright and frank discussion, the official said, adding "all the issues are being discussed."
Moscow brokered a ceasefire between Yerevan and Baku after the latest bout of fighting in 2020, and posted peacekeepers along the Lachin corridor.
With Russia bogged down in Ukraine and unwilling to strain ties with Azerbaijan's key ally Turkey, the United States and European Union have sought to steer a thaw in ties.
France's Foreign Minister Catherine Colonna visited the two countries last week aiming to cool down tensions over the border checkpoint.
She visited Baku and then Yerevan, urging Azerbaijan to restore "unhindered movement" through the Lachin corridor.
In Yerevan she said in a news conference that Armenia's territorial integrity must be respected.
"The purpose of the visit is to reaffirm France's support for the Armenian government and people," Colonna said.
But Azerbaijan reiterated that it had set up a checkpoint on "Azerbaijan's territory."
Colonna said it was important for Armenia and Azerbaijan to resume negotiations to secure a resolution to their decades-long standoff.
"We encourage you to resolutely take this path," Colonna said, adding this was "the only way to achieve a just and lasting peace."
Blinken has already taken part in two trilateral meetings with the two Caucasus rivals, in November last year and then again in February, on the margins of the international security conference in Munich, Germany.
On Saturday Blinken spoke with Armenia's Prime Minister Nikol Pashinyan, emphasizing the importance of peace discussions and pledging continued US support.
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