diff --git a/swh/lister/opam/lister.py b/swh/lister/opam/lister.py
--- a/swh/lister/opam/lister.py
+++ b/swh/lister/opam/lister.py
@@ -7,7 +7,7 @@
 import logging
 import os
 from subprocess import PIPE, Popen, call
-from typing import Iterator, Optional
+from typing import Any, Dict, Iterator, Optional
 
 from swh.lister.pattern import StatelessLister
 from swh.scheduler.interface import SchedulerInterface
@@ -53,24 +53,12 @@
         self.env = os.environ.copy()
         # Opam root folder is initialized in the :meth:`get_pages` method as no
         # side-effect should happen in the constructor to ease instantiation
-        self.opamroot = os.path.join(opam_root, self.instance)
+        self.opam_root = opam_root
 
     def get_pages(self) -> Iterator[PageType]:
-        # Initialize the opam root directory with the opam instance data to list.
-        call(
-            [
-                "opam",
-                "init",
-                "--reinit",
-                "--bare",
-                "--no-setup",
-                "--root",
-                self.opamroot,
-                self.instance,
-                self.url,
-            ],
-            env=self.env,
-        )
+        # Initialize the opam root directory
+        opam_init(self.opam_root, self.instance, self.url, self.env)
+
         # Actually list opam instance data
         proc = Popen(
             [
@@ -81,7 +69,7 @@
                 "--repos",
                 self.instance,
                 "--root",
-                self.opamroot,
+                self.opam_root,
                 "--normalise",
                 "--short",
             ],
@@ -103,9 +91,50 @@
             url=url,
             last_update=None,
             extra_loader_arguments={
-                "opam_root": self.opamroot,
+                "opam_root": self.opam_root,
                 "opam_instance": self.instance,
                 "opam_url": self.url,
                 "opam_package": page,
             },
         )
+
+
+def opam_init(opam_root: str, instance: str, url: str, env: Dict[str, Any]) -> None:
+    """Initialize an opam_root folder.
+
+    Args:
+        opam_root: The opam root folder to initialize
+        instance: Name of the opam repository to add or initialize
+        url: The associated url of the opam repository to add or initialize
+        env: The global environment to use for the opam command.
+
+    Returns:
+        None.
+
+    """
+    if not os.path.exists(opam_root) or not os.listdir(opam_root):
+        command = [
+            "opam",
+            "init",
+            "--reinit",
+            "--bare",
+            "--no-setup",
+            "--root",
+            opam_root,
+            instance,
+            url,
+        ]
+    else:
+        # The repository exists and is populated, we just add another instance in the
+        # repository. If it's already setup, it's a noop
+        command = [
+            "opam",
+            "repository",
+            "add",
+            "--root",
+            opam_root,
+            instance,
+            url,
+        ]
+    # Actually execute the command
+    call(command, env=env)
diff --git a/swh/lister/opam/tests/test_lister.py b/swh/lister/opam/tests/test_lister.py
--- a/swh/lister/opam/tests/test_lister.py
+++ b/swh/lister/opam/tests/test_lister.py
@@ -36,21 +36,19 @@
 
     lister = OpamLister(swh_scheduler, url=instance_url,)
     assert lister.instance == netloc
-    assert lister.opamroot.endswith(lister.instance)
+    assert lister.opam_root == "/tmp/opam/"
 
 
 def test_urls(swh_scheduler, mock_opam):
     mock_init, mock_popen = mock_opam
-
     instance_url = "https://opam.ocaml.org"
+    tmp_folder = mkdtemp(prefix="swh_opam_lister")
 
     lister = OpamLister(
-        swh_scheduler,
-        url=instance_url,
-        instance="opam",
-        opam_root=mkdtemp(prefix="swh_opam_lister"),
+        swh_scheduler, url=instance_url, instance="opam", opam_root=tmp_folder,
     )
     assert lister.instance == "opam"
+    assert lister.opam_root == tmp_folder
 
     # call the lister and get all listed origins urls
     stats = lister.run()
@@ -101,3 +99,32 @@
     result_urls = [origin.url for origin in scheduler_origins]
 
     assert expected_urls == result_urls
+
+
+def test_opam_multi_instance(datadir, swh_scheduler):
+    instance_url = f"file://{datadir}/fake_opam_repo"
+
+    lister = OpamLister(
+        swh_scheduler,
+        url=instance_url,
+        instance="fake",
+        opam_root=mkdtemp(prefix="swh_opam_lister"),
+    )
+
+    stats = lister.run()
+
+    assert stats.pages == 4
+    assert stats.origins == 4
+
+    scheduler_origins = swh_scheduler.get_listed_origins(lister.lister_obj.id).results
+
+    expected_urls = [
+        f"opam+{instance_url}/packages/agrid/",
+        f"opam+{instance_url}/packages/calculon/",
+        f"opam+{instance_url}/packages/directories/",
+        f"opam+{instance_url}/packages/ocb/",
+    ]
+
+    result_urls = [origin.url for origin in scheduler_origins]
+
+    assert expected_urls == result_urls