diff --git a/devtools/client/responsive/test/browser/browser.ini b/devtools/client/responsive/test/browser/browser.ini
index 5f68af1133c7..332e05dd90e4 100644
--- a/devtools/client/responsive/test/browser/browser.ini
+++ b/devtools/client/responsive/test/browser/browser.ini
@@ -53,6 +53,7 @@ tags = devtools webextensions
 [browser_mouse_resize.js]
 [browser_navigation.js]
 [browser_network_throttling.js]
+[browser_old-rdm_reload_conditions.js]
 [browser_orientationchange_event.js]
 [browser_page_redirection.js]
 skip-if = os == "linux"
diff --git a/devtools/client/responsive/test/browser/browser_old-rdm_reload_conditions.js b/devtools/client/responsive/test/browser/browser_old-rdm_reload_conditions.js
new file mode 100644
index 000000000000..36135eb5773e
--- /dev/null
+++ b/devtools/client/responsive/test/browser/browser_old-rdm_reload_conditions.js
@@ -0,0 +1,38 @@
+/* Any copyright is dedicated to the Public Domain.
+   http://creativecommons.org/publicdomain/zero/1.0/ */
+
+"use strict";
+
+// Verify that reload conditions restore old-RDM's tab to the proper state.
+// Bug 1585097: This test will be deleted once browser UI-enabled RDM is shipped to stable.
+
+const TEST_URL = "data:text/html;charset=utf-8,";
+
+addRDMTask(
+  null,
+  async function() {
+    info("Ensure reload conditions for touch simulation are enabled.");
+    reloadOnTouchChange(true);
+
+    const tab = await addTab(TEST_URL);
+    const { ui } = await openRDM(tab);
+    await toggleTouchSimulation(ui);
+
+    info("Wait for the UI's target to reload when opening RDM.");
+    await once(ui.currentTarget, "navigate");
+    ok(true, "RDM's tab target reloaded");
+
+    info("Wait for the tab to reload when closing RDM.");
+    const reloaded = BrowserTestUtils.waitForContentEvent(
+      tab.linkedBrowser,
+      "load",
+      true
+    );
+    await closeRDM(tab);
+    await reloaded;
+    ok(true, "Tab reloaded");
+
+    reloadOnTouchChange(false);
+  },
+  { usingBrowserUI: false, onlyPrefAndTask: true }
+);
diff --git a/devtools/client/responsive/ui.js b/devtools/client/responsive/ui.js
index 4403cb4b8978..b07d6a7a98b2 100644
--- a/devtools/client/responsive/ui.js
+++ b/devtools/client/responsive/ui.js
@@ -350,6 +350,8 @@ class ResponsiveUI {
         (options.reason === "TabClose" ||
           options.reason === "BeforeTabRemotenessChange"));
 
+    let currentTarget;
+
     // Ensure init has finished before starting destroy
     if (!isTabContentDestroying) {
       await this.inited;
@@ -365,6 +367,10 @@ class ResponsiveUI {
         this.hideBrowserUI();
       }
 
+      // Save reference to tab target before RDM stops listening to it. Will need it if
+      // the tab has to be reloaded to remove the emulated settings created by RDM.
+      currentTarget = this.currentTarget;
+
       this.targetList.unwatchTargets(
         [this.targetList.TYPES.FRAME],
         this.onTargetAvailable
@@ -416,8 +422,8 @@ class ResponsiveUI {
       reloadNeeded |=
         (await this.updateTouchSimulation()) &&
         this.reloadOnChange("touchSimulation");
-      if (reloadNeeded) {
-        this.getViewportBrowser().reload();
+      if (reloadNeeded && currentTarget) {
+        await currentTarget.reload();
       }
     }
 
@@ -604,7 +610,7 @@ class ResponsiveUI {
       (await this.updateTouchSimulation(touch)) &&
       this.reloadOnChange("touchSimulation");
     if (reloadNeeded) {
-      this.getViewportBrowser().reload();
+      this.reloadBrowser();
     }
     // Used by tests
     this.emit("device-changed");
@@ -631,7 +637,7 @@ class ResponsiveUI {
       (await this.updateTouchSimulation(enabled)) &&
       this.reloadOnChange("touchSimulation");
     if (reloadNeeded) {
-      this.getViewportBrowser().reload();
+      this.reloadBrowser();
     }
     // Used by tests
     this.emit("touch-simulation-changed");
@@ -643,7 +649,7 @@ class ResponsiveUI {
       (await this.updateUserAgent(userAgent)) &&
       this.reloadOnChange("userAgent");
     if (reloadNeeded) {
-      this.getViewportBrowser().reload();
+      this.reloadBrowser();
     }
     this.emit("user-agent-changed");
   }
@@ -670,7 +676,7 @@ class ResponsiveUI {
       (await this.updateTouchSimulation()) &&
       this.reloadOnChange("touchSimulation");
     if (reloadNeeded) {
-      this.getViewportBrowser().reload();
+      this.reloadBrowser();
     }
     // Used by tests
     this.emit("device-association-removed");
@@ -911,7 +917,7 @@ class ResponsiveUI {
         this.reloadOnChange("userAgent");
     }
     if (reloadNeeded) {
-      this.getViewportBrowser().reload();
+      this.reloadBrowser();
     }
   }
 
@@ -1197,6 +1203,13 @@ class ResponsiveUI {
       });
     }
   }
+
+  /**
+   * Reload the current tab.
+   */
+  async reloadBrowser() {
+    await this.currentTarget.reload();
+  }
 }
 
 module.exports = ResponsiveUI;