diff --git a/changes/pr3596.yaml b/changes/pr3596.yaml
new file mode 100644
index 000000000000..2fd493942642
--- /dev/null
+++ b/changes/pr3596.yaml
@@ -0,0 +1,5 @@
+enhancement:
+  - "Allow use of multiple image pull secrets in `KubernetesAgent`, `DaskKubernetesEnvironment` - [#3596](https://github.com/PrefectHQ/prefect/pull/3596)"
+
+contributor:
+  - "[James Lamb](https://github.com/jameslamb)"
diff --git a/src/prefect/agent/kubernetes/agent.py b/src/prefect/agent/kubernetes/agent.py
index 4f60d46234a7..8fac28a5ca72 100644
--- a/src/prefect/agent/kubernetes/agent.py
+++ b/src/prefect/agent/kubernetes/agent.py
@@ -303,7 +303,10 @@ def generate_job_spec_from_environment(
         - `IMAGE_PULL_POLICY`: policy for pulling images. Defaults to `"IfNotPresent"`.
         - `IMAGE_PULL_SECRETS`: name of an existing k8s secret that can be used to pull
                 images. This is necessary if your flow uses an image that is in a non-public
-                container registry, such as Amazon ECR.
+                container registry, such as Amazon ECR, or in a public registry that requires
+                authentication to avoid hitting rate limits. To specify multiple image pull
+                secrets, provide a comma-delimited string with no spaces, like
+                `"some-secret,other-secret"`.
         - `SERVICE_ACCOUNT_NAME`: name of a service account to run the job as.
                 By default, none is specified.
         - `YAML_TEMPLATE`: a path to where the YAML template should be loaded from. defaults
@@ -366,9 +369,19 @@ def generate_job_spec_from_environment(
         # Use image pull secrets if provided
         image_pull_secrets = os.getenv("IMAGE_PULL_SECRETS")
         if image_pull_secrets:
-            job["spec"]["template"]["spec"]["imagePullSecrets"][0][
-                "name"
-            ] = image_pull_secrets
+            secrets = image_pull_secrets.split(",")
+            for idx, secret_name in enumerate(secrets):
+                # this check preserves behavior from previous releases,
+                # where prefect would only overwrite the first entry in
+                # imagePullSecrets
+                if idx == 0:
+                    job["spec"]["template"]["spec"]["imagePullSecrets"][0] = {
+                        "name": secret_name
+                    }
+                else:
+                    job["spec"]["template"]["spec"]["imagePullSecrets"].append(
+                        {"name": secret_name}
+                    )
         else:
             del job["spec"]["template"]["spec"]["imagePullSecrets"]
 
diff --git a/src/prefect/environments/execution/dask/k8s.py b/src/prefect/environments/execution/dask/k8s.py
index 7d658ed665d7..8c2e2ebc28a0 100644
--- a/src/prefect/environments/execution/dask/k8s.py
+++ b/src/prefect/environments/execution/dask/k8s.py
@@ -79,7 +79,9 @@ class DaskKubernetesEnvironment(Environment):
         - scheduler_spec_file (str, optional): Path to a scheduler spec YAML file
         - worker_spec_file (str, optional): Path to a worker spec YAML file
         - image_pull_secret (str, optional): optional name of an `imagePullSecret` to use for
-            the scheduler and worker pods. For more information go
+            the scheduler and worker pods. To specify multiple image pull secrets, provide a comma
+            delimited string with no spaces, like `"some-secret,other-secret"`.
+            For more information go
             [here](https://kubernetes.io/docs/tasks/configure-pod-container/pull-image-private-registry/).
             `Warning`:  `image_pull_secret` if provided won't be appended to your custom
             `worker_spec_file` or `scheduler_spec_file`. If you want it, don't forget to add it in
@@ -389,7 +391,9 @@ def _populate_job_yaml(self, yaml_obj: dict, docker_name: str) -> dict:
             pod_spec["imagePullSecrets"].append({"name": namespace + "-docker"})
         elif self.image_pull_secret:
             pod_spec["imagePullSecrets"] = []
-            pod_spec["imagePullSecrets"].append({"name": self.image_pull_secret})
+            secrets = self.image_pull_secret.split(",")
+            for secret_name in secrets:
+                pod_spec["imagePullSecrets"].append({"name": secret_name})
 
         env[0]["value"] = prefect.config.cloud.graphql
         env[1]["value"] = prefect.config.cloud.auth_token
@@ -432,7 +436,9 @@ def _populate_worker_pod_yaml(self, yaml_obj: dict) -> dict:
             pod_spec["imagePullSecrets"].append({"name": namespace + "-docker"})
         elif self.image_pull_secret:
             pod_spec["imagePullSecrets"] = []
-            pod_spec["imagePullSecrets"].append({"name": self.image_pull_secret})
+            secrets = self.image_pull_secret.split(",")
+            for secret_name in secrets:
+                pod_spec["imagePullSecrets"].append({"name": secret_name})
 
         # set image
         yaml_obj["spec"]["containers"][0]["image"] = prefect.context.get(
diff --git a/tests/agent/test_k8s_agent.py b/tests/agent/test_k8s_agent.py
index dfe0a1be325f..35350edb6f68 100644
--- a/tests/agent/test_k8s_agent.py
+++ b/tests/agent/test_k8s_agent.py
@@ -273,6 +273,45 @@ def test_k8s_agent_replace_yaml_uses_user_env_vars(monkeypatch, cloud_api):
         )
         assert job["spec"]["template"]["spec"]["serviceAccountName"] == "svc_name"
 
+        assert job["spec"]["template"]["spec"]["imagePullSecrets"] == [
+            {"name": "my-secret"}
+        ]
+
+
+def test_k8s_agent_replace_yaml_respects_multiple_image_secrets(monkeypatch, cloud_api):
+    get_jobs = MagicMock(return_value=[])
+    monkeypatch.setattr(
+        "prefect.agent.kubernetes.agent.KubernetesAgent.manage_jobs",
+        get_jobs,
+    )
+
+    monkeypatch.setenv("IMAGE_PULL_SECRETS", "some-secret,other-secret")
+    monkeypatch.setenv("IMAGE_PULL_POLICY", "custom_policy")
+
+    flow_run = GraphQLResult(
+        {
+            "flow": GraphQLResult(
+                {
+                    "storage": Docker(
+                        registry_url="test", image_name="name", image_tag="tag"
+                    ).serialize(),
+                    "environment": LocalEnvironment().serialize(),
+                    "id": "new_id",
+                    "core_version": "0.13.0",
+                }
+            ),
+            "id": "id",
+        }
+    )
+
+    with set_temporary_config(
+        {"cloud.agent.auth_token": "token", "logging.log_to_cloud": True}
+    ):
+        agent = KubernetesAgent(env_vars=dict(AUTH_THING="foo", PKG_SETTING="bar"))
+        job = agent.generate_job_spec_from_environment(flow_run, image="test/name:tag")
+        expected_secrets = [{"name": "some-secret"}, {"name": "other-secret"}]
+        assert job["spec"]["template"]["spec"]["imagePullSecrets"] == expected_secrets
+
 
 def test_k8s_agent_replace_yaml(monkeypatch, cloud_api):
     get_jobs = MagicMock(return_value=[])
diff --git a/tests/environments/execution/test_dask_k8s_environment.py b/tests/environments/execution/test_dask_k8s_environment.py
index afd0e7513667..f34a5d1355ff 100644
--- a/tests/environments/execution/test_dask_k8s_environment.py
+++ b/tests/environments/execution/test_dask_k8s_environment.py
@@ -56,6 +56,20 @@ def test_create_dask_environment_args():
     assert environment.image_pull_secret == "secret"
 
 
+def test_create_dask_environment_multiple_image_secrets_in_args():
+    environment = DaskKubernetesEnvironment(
+        min_workers=5,
+        max_workers=6,
+        work_stealing=False,
+        scheduler_logs=True,
+        private_registry=True,
+        docker_secret="docker",
+        metadata={"test": "here"},
+        image_pull_secret="some-cred,different-cred",
+    )
+    assert environment.image_pull_secret == "some-cred,different-cred"
+
+
 def test_create_dask_environment_labels():
     environment = DaskKubernetesEnvironment(labels=["foo"])
     assert environment.labels == set(["foo"])
@@ -288,6 +302,32 @@ def test_populate_job_yaml():
     )
 
 
+def test_populate_job_yaml_multiple_image_secrets():
+    environment = DaskKubernetesEnvironment(
+        image_pull_secret="good-secret,dangerous-secret"
+    )
+
+    file_path = os.path.dirname(prefect.environments.execution.dask.k8s.__file__)
+
+    with open(path.join(file_path, "job.yaml")) as job_file:
+        job = yaml.safe_load(job_file)
+
+    with set_temporary_config(
+        {
+            "cloud.graphql": "gql_test",
+            "cloud.auth_token": "auth_test",
+            "logging.extra_loggers": ["test_logger"],
+        }
+    ):
+        with prefect.context(flow_run_id="id_test", namespace="namespace_test"):
+            yaml_obj = environment._populate_job_yaml(
+                yaml_obj=job, docker_name="test1/test2:test3"
+            )
+
+    expected_secrets = [dict(name="good-secret"), dict(name="dangerous-secret")]
+    assert yaml_obj["spec"]["template"]["spec"]["imagePullSecrets"] == expected_secrets
+
+
 def test_populate_worker_pod_yaml():
     environment = DaskKubernetesEnvironment()
 
@@ -363,6 +403,28 @@ def test_populate_worker_pod_yaml_with_image_pull_secret():
     yaml_obj["spec"]["imagePullSecrets"][0] == dict(name="mysecret")
 
 
+def test_populate_worker_pod_yaml_with_multiple_image_pull_secrets():
+    environment = DaskKubernetesEnvironment(image_pull_secret="some-secret,another-one")
+
+    file_path = os.path.dirname(prefect.environments.execution.dask.k8s.__file__)
+
+    with open(path.join(file_path, "worker_pod.yaml")) as pod_file:
+        pod = yaml.safe_load(pod_file)
+
+    with set_temporary_config(
+        {"cloud.graphql": "gql_test", "cloud.auth_token": "auth_test"}
+    ):
+        with prefect.context(
+            flow_run_id="id_test", image="my_image", namespace="foo-man"
+        ):
+            yaml_obj = environment._populate_worker_pod_yaml(yaml_obj=pod)
+
+    assert yaml_obj["spec"]["imagePullSecrets"] == [
+        dict(name="some-secret"),
+        dict(name="another-one"),
+    ]
+
+
 def test_initialize_environment_with_spec_populates(monkeypatch):
 
     with tempfile.TemporaryDirectory() as directory: