KABUL—When Abdullah, a Taliban commander in central Afghanistan, needs more rifles and ammunition, he turns to the same people who pay his $580-a-month salary: his Iranian sponsors.

“Iran supplies us with whatever we need,” he said.

Afghan and Western officials say Tehran has quietly increased its supply of weapons, ammunition and funding to the Taliban, and is now recruiting and training their fighters, posing a new threat to Afghanistan’s fragile security.

Iran’s strategy in backing the Taliban is twofold, these officials say: countering U.S. influence in the region and providing a counterweight to Islamic State’s move into the Taliban’s territory in Afghanistan.

The Taliban’s aggressive military push and the new momentum toward peace negotiations between them and Kabul also raises the possibility that some of their members could eventually return to power.

“Iran is betting on the re-emergence of the Taliban,” said a Western diplomat. “They are uncertain about where Afghanistan is heading right now, so they are hedging their bets.”

Iranian officials didn’t respond to requests for comment, but Tehran has repeatedly denied providing financial or military aid to the Taliban in conversations with Afghan and Western officials. “Whenever we discussed it, they would deny it,” a former senior Afghan official said.

The developing Iran-Taliban alliance represents a new complication in Mr. Obama’s plans for both the Middle East and the future of Afghanistan, where the U.S. has been working to curb the Taliban’s role ahead of a planned withdrawal of all but 1,000 U.S. troops at the end of his presidency in 2016. At its peak in 2011 there were 100,000 U.S. troops.

The White House-supported international nuclear talks with Iran that are scheduled to finish this month face world-wide criticism for potentially setting up a new regional dynamic in which Tehran, unfettered by punitive economic sanctions and flush with new resources, would be able to pursue an activist agenda through its proxies in and around the Middle East. Tehran’s growing ties to the Taliban is another sign of that, these critics say.

Rep. Ed Royce (R., Calif.), chairman of the House Foreign Affairs Committee, said Iran’s support to the Taliban could increase if a nuclear deal is signed and Iran wins sanction relief.

“Across the region, Iran is stepping up its support for militants and rebel groups,” Mr. Royce said. “With billions in sanctions relief coming, that support goes into overdrive.”

Sen. John McCain (R., Ariz), chairman of the Armed Services Committee, said Iran’s increased support to the Taliban is a continuation of its aggressive behavior in Yemen, Syria, Iraq and Lebanon. “This is further evidence of the administration’s continued willful disregard for the facts on the ground in light of Iranian aggression in the region,” he said.

U.S. officials declined to comment specifically about closer Iran-Taliban ties, but have said that its diplomacy with Iran doesn’t alter its concerns about Iran’s destabilizing influence in the region. Director of National Intelligence James Clapper said in a recent letter to lawmakers that Iran was the “foremost state sponsor of terrorism.”

The Taliban have long used Pakistani territory as their main recruiting base and headquarters. But Afghan and Western officials say Iran, through its elite Revolutionary Guard Corps, has emerged as an important ally for the Taliban.

What’s more, they say, Tehran is turning to Afghan immigrants within its borders—a tactic it has also used to find new recruits to fight in support of President Bashar al-Assad’s regime in Syria.

Mr. Abdullah is one of those Iranian-backed Taliban fighters. After being detained for working as an illegal laborer in the Iranian port city of Bandar Abbas, Mr. Abdullah said he was approached by an Iranian intelligence officer.

“He asked me how much money I made, and that he would double my salary if I went to work for them in Afghanistan,” he said.

Mr. Abdullah said smugglers hired by Iran ferry supplies across the lawless borderlands where Iran, Afghanistan and Pakistan meet and deliver them to Taliban units in Afghan territory. He said his fighters receive weapons that include 82mm mortars, light machine guns, AK-47 rifles, rocket-propelled grenades and materials for making roadside bombs.

Military and intelligence officials see Iran’s support to the Taliban as an alliance of convenience. Historically, relations between Iran, a Shiite theocracy, and the hard-line Sunni Taliban have been fraught. Iran nearly went to war against the Taliban regime in 1998 after 10 of its diplomats were killed when their consulate in the northern Afghan city of Mazar-e Sharif was overrun.

Iran didn’t oppose the overthrow of the Taliban in 2001, and it has since maintained friendly relations with the Western-backed government in Kabul.

But Iran has long been uneasy with the U.S. military presence on its doorstep, and the Revolutionary Guard Corps have been delivering weapons to the Taliban since at least 2007, according to an October 2014 report by the U.S. Department of Defense.

Iran’s alliance with the Taliban took a new turn in June 2013 when Tehran formally invited a Taliban delegation to participate in a conference on Islam and to meet senior Iranian officials.

By the fall of that year, Afghan security officials said they had clear evidence that Iran was training Taliban fighters within its borders. Tehran now operates at least four Taliban training camps, according to Afghan officials and Mr. Abdullah, the Taliban commander. They are in the Iranian cities of Tehran, Mashhad and Zahedan and in the province of Kerman.

“At the beginning Iran was supporting Taliban financially,” said a senior Afghan official. “But now they are training and equipping them, too.”

The drawdown of U.S. and allied troops has made it easier for Taliban fighters and smugglers to cross the porous border undetected. “In the past, the U.S. had significant surveillance capabilities,” said Sayed Wahid Qattali, an influential politician from the western city Herat, where Iran has long had influence. “But now that the Americans have left, Iran is a lot freer.”

Iran formalized its alliance with the Taliban by allowing the group to open an office in Mashhad, maintaining a presence there since at least the beginning of 2014, a foreign official said. The office has gained so much clout that some foreign officials are now referring to it as the “Mashhad Shura,” a term used to describe the Taliban’s leadership councils.

One of the main points of contact between Tehran and the insurgency is head of the Taliban’s Qatar-based political office, Tayeb Agha, Afghan and foreign officials said. His most recent trip to Iran was in mid-May, the insurgent group said. The Taliban deny they receive support from Iran or any other foreign country, but say they want good relations with Afghanistan’s neighbors.

Iran’s backing of the Taliban has a strategic rationale. Tehran is already battling Islamic State, also known as Daesh, in Syria and Iraq, and it is wary of a new front line emerging close to its eastern border, Afghan officials say.

“Iran seeks to counter Daesh with the Taliban,” said an Afghan security official.

For the Taliban, Islamic State militants represent a threat of a different kind: they are competitors. Since an offshoot of Islamic State announced plans to expand in Afghanistan and Pakistan earlier this year, the new group has been actively recruiting fighters, many of whom are disaffected Taliban, say residents and Afghan officials.

This has pitted the two rival jihadist groups against each other, with clashes erupting between them in provinces including Helmand in the south, Nangarhar in the east and specifically involving Iran-backed Taliban in Farah, near Iran’s border, Afghan officials say.

Iranian funding gives more options to the militant group, support that is beginning to have an impact on the battlefield.

“If it wasn’t for Iran, I don’t think they would’ve been able to push an offensive like they are doing now,” said Antonio Giustozzi, a Taliban expert who has tracked Iran’s involvement in Afghanistan.

In recent months, security in Afghanistan’s west and north deteriorated sharply compared to last year, as Taliban fighters amassed in large numbers, testing the ability of Afghan troops to hold their ground.

It’s unclear, however, how far Iran will go to promote the Taliban.

“They wouldn’t want the Taliban to become too strong,” said a second foreign official. “They just want to make sure that they have some levers in their hands, because if the Taliban would win, God forbid, then they would lose all their leverage.”

WSJ