diff --git a/scripts/pylib/pytest-twister-harness/src/twister_harness/device/device_adapter.py b/scripts/pylib/pytest-twister-harness/src/twister_harness/device/device_adapter.py
index b5560650c1b..3f73045f899 100644
--- a/scripts/pylib/pytest-twister-harness/src/twister_harness/device/device_adapter.py
+++ b/scripts/pylib/pytest-twister-harness/src/twister_harness/device/device_adapter.py
@@ -14,6 +14,7 @@ import threading
 import time
 from datetime import datetime
 from pathlib import Path
+from serial import SerialException
 
 from twister_harness.exceptions import (
     TwisterHarnessException,
@@ -69,14 +70,23 @@ class DeviceAdapter(abc.ABC):
 
         if self.device_config.type != 'hardware':
             self._flash_and_run()
+            self._device_run.set()
+            self._start_reader_thread()
+            self.connect()
+            return
 
         self._device_run.set()
         self._start_reader_thread()
-        self.connect()
 
-        if self.device_config.type == 'hardware':
+        if self.device_config.flash_before:
+            # For hardware devices with shared USB or software USB, connect after flashing.
+            # Retry for up to 10 seconds for USB-CDC based devices to enumerate.
+            self._flash_and_run()
+            self.connect(retry_s = 10)
+        else:
             # On hardware, flash after connecting to COM port, otherwise some messages
             # from target can be lost.
+            self.connect()
             self._flash_and_run()
 
     def close(self) -> None:
@@ -89,7 +99,7 @@ class DeviceAdapter(abc.ABC):
         self._device_run.clear()
         self._join_reader_thread()
 
-    def connect(self) -> None:
+    def connect(self, retry_s: int = 0) -> None:
         """Connect to device - allow for output gathering."""
         if self.is_device_connected():
             logger.debug('Device already connected')
@@ -98,7 +108,20 @@ class DeviceAdapter(abc.ABC):
             msg = 'Cannot connect to not working device'
             logger.error(msg)
             raise TwisterHarnessException(msg)
-        self._connect_device()
+
+        if retry_s > 0:
+            retry_cycles = retry_s * 10
+            for i in range(retry_cycles):
+                try:
+                    self._connect_device()
+                    break
+                except SerialException:
+                    if i == retry_cycles - 1:
+                        raise
+                    time.sleep(0.1)
+        else:
+            self._connect_device()
+
         self._device_connected.set()
 
     def disconnect(self) -> None:
diff --git a/scripts/pylib/pytest-twister-harness/src/twister_harness/plugin.py b/scripts/pylib/pytest-twister-harness/src/twister_harness/plugin.py
index 34a09aa38f5..60537608357 100644
--- a/scripts/pylib/pytest-twister-harness/src/twister_harness/plugin.py
+++ b/scripts/pylib/pytest-twister-harness/src/twister_harness/plugin.py
@@ -84,6 +84,13 @@ def pytest_addoption(parser: pytest.Parser):
         '--device-serial-pty',
         help='Script for controlling pseudoterminal.'
     )
+    twister_harness_group.addoption(
+        '--flash-before',
+        type=bool,
+        help='Flash device before attaching to serial port'
+             'This is useful for devices that share the same port for programming'
+             'and serial console, or use soft-USB, where flash must come first.'
+    )
     twister_harness_group.addoption(
         '--west-flash-extra-args',
         help='Extend parameters for west flash. '
diff --git a/scripts/pylib/pytest-twister-harness/src/twister_harness/twister_harness_config.py b/scripts/pylib/pytest-twister-harness/src/twister_harness/twister_harness_config.py
index ece190c630f..6ab26c3e8f4 100644
--- a/scripts/pylib/pytest-twister-harness/src/twister_harness/twister_harness_config.py
+++ b/scripts/pylib/pytest-twister-harness/src/twister_harness/twister_harness_config.py
@@ -26,6 +26,7 @@ class DeviceConfig:
     id: str = ''
     product: str = ''
     serial_pty: str = ''
+    flash_before: bool = False
     west_flash_extra_args: list[str] = field(default_factory=list, repr=False)
     name: str = ''
     pre_script: Path | None = None
@@ -62,6 +63,7 @@ class TwisterHarnessConfig:
             id=config.option.device_id,
             product=config.option.device_product,
             serial_pty=config.option.device_serial_pty,
+            flash_before=bool(config.option.flash_before),
             west_flash_extra_args=west_flash_extra_args,
             pre_script=_cast_to_path(config.option.pre_script),
             post_script=_cast_to_path(config.option.post_script),
diff --git a/scripts/pylib/twister/twisterlib/environment.py b/scripts/pylib/twister/twisterlib/environment.py
index dcd8fe9189c..85b7cdb371e 100644
--- a/scripts/pylib/twister/twisterlib/environment.py
+++ b/scripts/pylib/twister/twisterlib/environment.py
@@ -178,7 +178,7 @@ Artificially long but functional example:
     parser.add_argument("--flash-before", action="store_true", default=False,
                         help="""Flash device before attaching to serial port.
                         This is useful for devices that share the same port for programming
-                        and serial console, where flash must come first.
+                        and serial console, or use soft-USB, where flash must come first.
                         """)
 
     test_or_build.add_argument(
diff --git a/scripts/pylib/twister/twisterlib/harness.py b/scripts/pylib/twister/twisterlib/harness.py
index 6fd6dae73a8..b0925c0fce0 100644
--- a/scripts/pylib/twister/twisterlib/harness.py
+++ b/scripts/pylib/twister/twisterlib/harness.py
@@ -408,6 +408,9 @@ class Pytest(Harness):
         if hardware.post_script:
             command.append(f'--post-script={hardware.post_script}')
 
+        if hardware.flash_before:
+            command.append(f'--flash-before={hardware.flash_before}')
+
         return command
 
     def run_command(self, cmd, timeout):