diff --git a/ecs-agent/netlib/platform/common_linux.go b/ecs-agent/netlib/platform/common_linux.go
index 2b8bb0a4829..98a80d01860 100644
--- a/ecs-agent/netlib/platform/common_linux.go
+++ b/ecs-agent/netlib/platform/common_linux.go
@@ -566,10 +566,54 @@ func (c *common) createResolvConf(netNSDir string,
 		return err
 	}
 
-	// Copy Host's resolv.conf file.
-	return c.copyFile(filepath.Join(netNSDir, ResolveConfFileName),
-		filepath.Join(c.resolvConfPath, ResolveConfFileName),
-		taskDNSConfigFileMode)
+	// Copy Host's resolv.conf file and backfill DNS fields on the interface
+	// so downstream consumers can read DNS config from the model.
+	src := filepath.Join(c.resolvConfPath, ResolveConfFileName)
+	contents, err := c.ioutil.ReadFile(src)
+	if err != nil {
+		return errors.Wrapf(err, "unable to read %s", src)
+	}
+	dst := filepath.Join(netNSDir, ResolveConfFileName)
+	if err := c.ioutil.WriteFile(dst, contents, taskDNSConfigFileMode); err != nil {
+		return errors.Wrapf(err, "unable to write to %s", dst)
+	}
+	servers, searches := parseResolvConf(contents)
+	iface.DomainNameServers = servers
+	iface.DomainNameSearchList = searches
+	return nil
+}
+
+// parseResolvConf extracts nameserver addresses and search domains from content
+// in the resolv.conf(5) format.
+//
+// Parsing rules (matching the behavior of Go's net.dnsReadConfig in
+// src/net/dnsconfig_unix.go and glibc's res_init):
+//   - Lines starting with ';' or '#' are treated as comments and skipped.
+//   - Fields are separated by any combination of spaces and tabs.
+//   - A "nameserver" line contributes one IP address (the second field).
+//   - A "search" line contributes all subsequent fields as search domains;
+//     if multiple search lines appear, only the last is used.
+//   - All other directives are ignored.
+func parseResolvConf(content []byte) (servers, searches []string) {
+	for _, line := range bytes.Split(content, []byte("\n")) {
+		if len(line) == 0 || line[0] == ';' || line[0] == '#' {
+			continue
+		}
+		fields := bytes.Fields(line)
+		if len(fields) < 2 {
+			continue
+		}
+		switch string(fields[0]) {
+		case "nameserver":
+			servers = append(servers, string(fields[1]))
+		case "search":
+			searches = nil
+			for _, f := range fields[1:] {
+				searches = append(searches, string(f))
+			}
+		}
+	}
+	return servers, searches
 }
 
 func (c *common) copyFile(dst, src string, fileMode os.FileMode) error {
diff --git a/ecs-agent/netlib/platform/common_linux_test.go b/ecs-agent/netlib/platform/common_linux_test.go
index 5866f5dcbd3..f4d2916cb6b 100644
--- a/ecs-agent/netlib/platform/common_linux_test.go
+++ b/ecs-agent/netlib/platform/common_linux_test.go
@@ -606,3 +606,78 @@ func TestParseHosts(t *testing.T) {
 		})
 	}
 }
+
+func TestParseResolvConf(t *testing.T) {
+	tests := []struct {
+		name            string
+		input           string
+		expectedServers []string
+		expectedSearch  []string
+	}{
+		{
+			// Test fixture from Go's net package resolv.conf parser tests:
+			// https://github.com/golang/go/blob/master/src/net/testdata/resolv.conf
+			name: "Go stdlib test fixture",
+			input: "# /etc/resolv.conf\n" +
+				"domain localdomain\n" +
+				"nameserver 8.8.8.8\n" +
+				"nameserver 2001:4860:4860::8888\n" +
+				"nameserver fe80::1%lo0\n" +
+				"options ndots:5 timeout:10 attempts:3 rotate\n" +
+				"options attempts 3\n",
+			expectedServers: []string{"8.8.8.8", "2001:4860:4860::8888", "fe80::1%lo0"},
+			expectedSearch:  nil,
+		},
+		{
+			name:            "semicolon comments",
+			input:           "; this is a comment\nnameserver 8.8.8.8\n",
+			expectedServers: []string{"8.8.8.8"},
+			expectedSearch:  nil,
+		},
+		{
+			name:            "tabs as separators",
+			input:           "nameserver\t10.0.0.2\nsearch\tlocal\texample.com\n",
+			expectedServers: []string{"10.0.0.2"},
+			expectedSearch:  []string{"local", "example.com"},
+		},
+		{
+			name:            "multiple spaces between keyword and value",
+			input:           "nameserver   8.8.8.8\nsearch   example.com\n",
+			expectedServers: []string{"8.8.8.8"},
+			expectedSearch:  []string{"example.com"},
+		},
+		{
+			name: "last search directive wins",
+			input: "search first.com\n" +
+				"search second.com third.com\n",
+			expectedServers: nil,
+			expectedSearch:  []string{"second.com", "third.com"},
+		},
+		{
+			name:            "empty input",
+			input:           "",
+			expectedServers: nil,
+			expectedSearch:  nil,
+		},
+		{
+			name:            "only comments and blanks",
+			input:           "# comment\n\n; another\n",
+			expectedServers: nil,
+			expectedSearch:  nil,
+		},
+		{
+			name:            "unknown directives ignored",
+			input:           "options ndots:5\nnameserver 10.0.0.2\ndomain example.com\nsortlist 130.155.160.0\n",
+			expectedServers: []string{"10.0.0.2"},
+			expectedSearch:  nil,
+		},
+	}
+
+	for _, tc := range tests {
+		t.Run(tc.name, func(t *testing.T) {
+			servers, searches := parseResolvConf([]byte(tc.input))
+			assert.Equal(t, tc.expectedServers, servers)
+			assert.Equal(t, tc.expectedSearch, searches)
+		})
+	}
+}