diff --git a/drivers/mspi/Kconfig.dw b/drivers/mspi/Kconfig.dw
index 06d2e09c8af..cff148c138c 100644
--- a/drivers/mspi/Kconfig.dw
+++ b/drivers/mspi/Kconfig.dw
@@ -12,6 +12,15 @@ config MSPI_DW
 
 if MSPI_DW
 
+config MSPI_DW_HANDLE_FIFOS_IN_SYSTEM_WORKQUEUE
+	bool "Handle FIFO in system workqueue"
+	help
+	  When the driver does not use DMA for transferring data to/from the
+	  SSI FIFOs, handling of those may take a significant amount of time.
+	  It may be destructive for some applications if that time is spent
+	  in the interrupt context. This option allows offloading the job to
+	  the system workqueue.
+
 config MSPI_DW_TXD_DIV
 	int "Designware SSI TX Drive edge divisor"
 	default 4
diff --git a/drivers/mspi/mspi_dw.c b/drivers/mspi/mspi_dw.c
index 66f257839aa..f1195314c6c 100644
--- a/drivers/mspi/mspi_dw.c
+++ b/drivers/mspi/mspi_dw.c
@@ -71,6 +71,12 @@ struct mspi_dw_data {
 	/* For locking of controller configuration. */
 	struct k_sem cfg_lock;
 	struct mspi_xfer xfer;
+
+#if defined(CONFIG_MSPI_DW_HANDLE_FIFOS_IN_SYSTEM_WORKQUEUE)
+	struct k_work fifo_work;
+	const struct device *dev;
+	uint32_t imr;
+#endif
 };
 
 struct mspi_dw_config {
@@ -111,7 +117,7 @@ DEFINE_MM_REG_RD_WR(rxftlr,	0x1c)
 DEFINE_MM_REG_RD(txflr,		0x20)
 DEFINE_MM_REG_RD(rxflr,		0x24)
 DEFINE_MM_REG_RD(sr,		0x28)
-DEFINE_MM_REG_WR(imr,		0x2c)
+DEFINE_MM_REG_RD_WR(imr,	0x2c)
 DEFINE_MM_REG_RD(isr,		0x30)
 DEFINE_MM_REG_RD(risr,		0x34)
 DEFINE_MM_REG_RD_WR(dr,		0x60)
@@ -218,6 +224,8 @@ static bool tx_dummy_bytes(const struct device *dev)
 		write_dr(dev, dummy_val);
 	} while (--dummy_bytes);
 
+	dev_data->dummy_bytes = 0;
+
 	/* Set the TX start level to 0, so that the transmission will be
 	 * started now if it hasn't been yet. The threshold value is also
 	 * set to 0 here, but it doesn't really matter, as the interrupt
@@ -280,7 +288,18 @@ static bool read_rx_fifo(const struct device *dev,
 	return false;
 }
 
-static void mspi_dw_isr(const struct device *dev)
+static inline void set_imr(const struct device *dev, uint32_t imr)
+{
+#if defined(CONFIG_MSPI_DW_HANDLE_FIFOS_IN_SYSTEM_WORKQUEUE)
+	struct mspi_dw_data *dev_data = dev->data;
+
+	dev_data->imr = imr;
+#else
+	write_imr(dev, imr);
+#endif
+}
+
+static void handle_fifos(const struct device *dev)
 {
 	struct mspi_dw_data *dev_data = dev->data;
 	const struct mspi_xfer_packet *packet =
@@ -302,42 +321,82 @@ static void mspi_dw_isr(const struct device *dev)
 			finished = true;
 		}
 	} else {
-		uint32_t int_status = read_isr(dev);
+		for (;;) {
+			/* Use RISR, not ISR, because when this function is
+			 * executed through the system workqueue, all interrupts
+			 * are masked (IMR is 0).
+			 */
+			uint32_t int_status = read_risr(dev);
 
-		do {
-			if (int_status & ISR_RXFIS_BIT) {
+			if (int_status & RISR_RXFIR_BIT) {
 				if (read_rx_fifo(dev, packet)) {
 					finished = true;
 					break;
 				}
 
-				if (read_risr(dev) & RISR_RXOIR_BIT) {
+				if (int_status & RISR_RXOIR_BIT) {
 					finished = true;
 					break;
 				}
 
-				int_status = read_isr(dev);
+				/* Refresh interrupt status, as during reading
+				 * from the RX FIFO, the TX FIFO status might
+				 * have changed.
+				 */
+				int_status = read_risr(dev);
 			}
 
-			if (int_status & ISR_TXEIS_BIT) {
-				if (tx_dummy_bytes(dev)) {
-					/* All the required dummy bytes were
-					 * written to the FIFO; disable the TXE
-					 * interrupt, as it's no longer needed.
-					 */
-					write_imr(dev, IMR_RXFIM_BIT);
-				}
+			if (dev_data->dummy_bytes == 0 ||
+			    !(int_status & RISR_TXEIR_BIT)) {
+				break;
+			}
 
-				int_status = read_isr(dev);
+			if (tx_dummy_bytes(dev)) {
+				/* All the required dummy bytes were written
+				 * to the FIFO; disable the TXE interrupt,
+				 * as it's no longer needed.
+				 */
+				set_imr(dev, IMR_RXFIM_BIT);
 			}
-		} while (int_status != 0);
+		}
 	}
 
 	if (finished) {
-		write_imr(dev, 0);
+		set_imr(dev, 0);
 
 		k_sem_give(&dev_data->finished);
 	}
+}
+
+#if defined(CONFIG_MSPI_DW_HANDLE_FIFOS_IN_SYSTEM_WORKQUEUE)
+static void fifo_work_handler(struct k_work *work)
+{
+	struct mspi_dw_data *dev_data =
+		CONTAINER_OF(work, struct mspi_dw_data, fifo_work);
+	const struct device *dev = dev_data->dev;
+
+	handle_fifos(dev);
+
+	write_imr(dev, dev_data->imr);
+}
+#endif
+
+static void mspi_dw_isr(const struct device *dev)
+{
+#if defined(CONFIG_MSPI_DW_HANDLE_FIFOS_IN_SYSTEM_WORKQUEUE)
+	struct mspi_dw_data *dev_data = dev->data;
+	int rc;
+
+	dev_data->imr = read_imr(dev);
+	write_imr(dev, 0);
+
+	rc = k_work_submit(&dev_data->fifo_work);
+	if (rc < 0) {
+		LOG_ERR("k_work_submit failed: %d\n", rc);
+	}
+#else
+	handle_fifos(dev);
+#endif
 
 	vendor_specific_irq_clear(dev);
 }
@@ -1426,6 +1485,11 @@ static int dev_init(const struct device *dev)
 	k_sem_init(&dev_data->cfg_lock, 1, 1);
 	k_sem_init(&dev_data->ctx_lock, 1, 1);
 
+#if defined(CONFIG_MSPI_DW_HANDLE_FIFOS_IN_SYSTEM_WORKQUEUE)
+	dev_data->dev = dev;
+	k_work_init(&dev_data->fifo_work, fifo_work_handler);
+#endif
+
 	for (ce_gpio = dev_config->ce_gpios;
 	     ce_gpio < &dev_config->ce_gpios[dev_config->ce_gpios_len];
 	     ce_gpio++) {
diff --git a/tests/drivers/mspi/flash/boards/nrf54h20dk_nrf54h20_cpuapp.overlay b/tests/drivers/mspi/flash/boards/nrf54h20dk_nrf54h20_cpuapp.overlay
new file mode 100644
index 00000000000..6e0d84e07cd
--- /dev/null
+++ b/tests/drivers/mspi/flash/boards/nrf54h20dk_nrf54h20_cpuapp.overlay
@@ -0,0 +1,23 @@
+/*
+ * Copyright (c) 2025 Nordic Semiconductor ASA
+ *
+ * SPDX-License-Identifier: Apache-2.0
+ */
+
+/ {
+	aliases {
+		mspi0 = &exmif;
+	};
+};
+
+&gpio6 {
+	status = "okay";
+};
+
+&exmif {
+	status = "okay";
+};
+
+&mx25uw63 {
+	status = "okay";
+};
diff --git a/tests/drivers/mspi/flash/testcase.yaml b/tests/drivers/mspi/flash/testcase.yaml
index 72755fd2aa4..dba610a4023 100644
--- a/tests/drivers/mspi/flash/testcase.yaml
+++ b/tests/drivers/mspi/flash/testcase.yaml
@@ -1,16 +1,18 @@
 # Copyright (c) 2024 Ambiq Micro Inc. <www.ambiq.com>
 # SPDX-License-Identifier: Apache-2.0
 
+common:
+  tags:
+    - drivers
+    - mspi
+    - flash
+  harness: ztest
+
 tests:
   drivers.mspi.flash:
-    tags:
-      - drivers
-      - mspi
-      - flash
     filter: dt_compat_enabled("zephyr,mspi-emul-flash")
       or dt_compat_enabled("jedec,spi-nor") or dt_compat_enabled("jedec,mspi-nor")
       or dt_compat_enabled("mspi-atxp032") or dt_compat_enabled("mspi-is25xX0xx")
-    harness: ztest
     platform_allow:
       - native_sim
       - apollo3p_evb
@@ -20,15 +22,17 @@ tests:
       - apollo3p_evb
       - apollo510_evb
   drivers.mspi.flash.xip_read:
-    tags:
-      - drivers
-      - mspi
-      - flash
     filter: dt_compat_enabled("mspi-is25xX0xx")
-    harness: ztest
     platform_allow:
       - apollo510_evb
     integration_platforms:
       - apollo510_evb
     extra_configs:
       - CONFIG_FLASH_MSPI_XIP_READ=y
+  drivers.mspi.flash.mspi_dw_system_workqueue:
+    filter: dt_alias_exists("mspi0") and dt_compat_enabled("jedec,mspi-nor")
+      and CONFIG_MSPI_DW
+    integration_platforms:
+      - nrf54h20dk/nrf54h20/cpuapp
+    extra_configs:
+      - CONFIG_MSPI_DW_HANDLE_FIFOS_IN_SYSTEM_WORKQUEUE=y