diff --git a/app/javascript/dashboard/components-next/Conversation/SidepanelSwitch.vue b/app/javascript/dashboard/components-next/Conversation/SidepanelSwitch.vue
index 5e96df3c6..779165caa 100644
--- a/app/javascript/dashboard/components-next/Conversation/SidepanelSwitch.vue
+++ b/app/javascript/dashboard/components-next/Conversation/SidepanelSwitch.vue
@@ -57,7 +57,7 @@ useKeyboardEvents(keyboardEvents);
 
 <template>
   <ButtonGroup
-    class="flex flex-col justify-center items-center absolute top-36 xl:top-24 ltr:right-2 rtl:left-2 bg-n-solid-2/90 backdrop-blur-lg border border-n-weak/50 rounded-full gap-1.5 p-1.5 shadow-sm transition-shadow duration-200 hover:shadow"
+    class="flex flex-col justify-center items-center absolute top-36 xl:top-24 ltr:right-2 rtl:left-2 bg-n-solid-2/90 backdrop-blur-lg border border-n-weak/50 rounded-full gap-1.5 p-1.5 shadow-sm transition-shadow duration-200 hover:shadow !z-20"
   >
     <Button
       v-tooltip.top="$t('CONVERSATION.SIDEBAR.CONTACT')"
diff --git a/app/javascript/dashboard/components/widgets/WootWriter/CopilotEditor.vue b/app/javascript/dashboard/components/widgets/WootWriter/CopilotEditor.vue
index cb4c93932..964645fbb 100644
--- a/app/javascript/dashboard/components/widgets/WootWriter/CopilotEditor.vue
+++ b/app/javascript/dashboard/components/widgets/WootWriter/CopilotEditor.vue
@@ -27,10 +27,6 @@ const props = defineProps({
     type: Boolean,
     default: true,
   },
-  isPopout: {
-    type: Boolean,
-    default: false,
-  },
 });
 
 const emit = defineEmits([
@@ -208,10 +204,7 @@ onMounted(() => {
 
 <template>
   <div class="space-y-2 mb-4">
-    <div
-      class="overflow-y-auto"
-      :class="{ 'max-h-96': isPopout, 'max-h-56': !isPopout }"
-    >
+    <div class="overflow-y-auto max-h-56">
       <p
         v-dompurify-html="formatMessage(generatedContent, false)"
         class="text-n-iris-12 text-sm prose-sm font-normal !mb-4"
diff --git a/app/javascript/dashboard/components/widgets/WootWriter/Editor.vue b/app/javascript/dashboard/components/widgets/WootWriter/Editor.vue
index 1bf08d169..e776ed913 100644
--- a/app/javascript/dashboard/components/widgets/WootWriter/Editor.vue
+++ b/app/javascript/dashboard/components/widgets/WootWriter/Editor.vue
@@ -984,7 +984,32 @@ useEmitter(BUS_EVENTS.INSERT_INTO_RICH_EDITOR, insertContentIntoEditor);
 }
 
 .ProseMirror-woot-style {
-  @apply overflow-auto min-h-[5rem] max-h-[7.5rem];
+  @apply overflow-auto;
+}
+
+.ProseMirror-woot-style:not(
+    :where(.resizable-editor-wrapper .ProseMirror-woot-style)
+  ) {
+  @apply min-h-[5rem] max-h-[7.5rem];
+}
+
+// Resizable editor wrapper styles
+.resizable-editor-wrapper {
+  .ProseMirror-woot-style {
+    min-height: clamp(
+      var(--editor-min-allowed, var(--editor-min-height, 5rem)),
+      var(--editor-height, var(--editor-min-height, 5rem)),
+      var(--editor-max-allowed, var(--editor-max-height, 7.5rem))
+    );
+    max-height: clamp(
+      var(--editor-min-allowed, var(--editor-min-height, 5rem)),
+      var(--editor-height, var(--editor-min-height, 5rem)),
+      var(--editor-max-allowed, var(--editor-max-height, 7.5rem))
+    );
+    transition:
+      min-height var(--editor-height-transition, 180ms ease),
+      max-height var(--editor-height-transition, 180ms ease);
+  }
 }
 
 .ProseMirror-prompt-backdrop::backdrop {
diff --git a/app/javascript/dashboard/components/widgets/WootWriter/ReplyTopPanel.vue b/app/javascript/dashboard/components/widgets/WootWriter/ReplyTopPanel.vue
index 210741481..cdf577c21 100644
--- a/app/javascript/dashboard/components/widgets/WootWriter/ReplyTopPanel.vue
+++ b/app/javascript/dashboard/components/widgets/WootWriter/ReplyTopPanel.vue
@@ -54,7 +54,7 @@ export default {
       default: undefined,
     },
   },
-  emits: ['setReplyMode', 'togglePopout', 'executeCopilotAction'],
+  emits: ['setReplyMode', 'toggleEditorSize', 'executeCopilotAction'],
   setup(props, { emit }) {
     const setReplyMode = mode => {
       emit('setReplyMode', mode);
@@ -189,7 +189,7 @@ export default {
         class="text-n-slate-11"
         sm
         icon="i-lucide-maximize-2"
-        @click="$emit('togglePopout')"
+        @click="$emit('toggleEditorSize')"
       />
     </div>
   </div>
diff --git a/app/javascript/dashboard/components/widgets/conversation/CopilotEditorSection.vue b/app/javascript/dashboard/components/widgets/conversation/CopilotEditorSection.vue
index bdd537d92..17d6712d4 100644
--- a/app/javascript/dashboard/components/widgets/conversation/CopilotEditorSection.vue
+++ b/app/javascript/dashboard/components/widgets/conversation/CopilotEditorSection.vue
@@ -16,10 +16,6 @@ defineProps({
     type: String,
     default: '',
   },
-  isPopout: {
-    type: Boolean,
-    default: false,
-  },
 });
 
 const emit = defineEmits([
@@ -69,7 +65,6 @@ const onSend = () => {
       :generated-content="generatedContent"
       :min-height="4"
       :enabled-menu-options="[]"
-      :is-popout="isPopout"
       @focus="onFocus"
       @blur="onBlur"
       @clear-selection="clearEditorSelection"
diff --git a/app/javascript/dashboard/components/widgets/conversation/MessagesView.vue b/app/javascript/dashboard/components/widgets/conversation/MessagesView.vue
index bc0b6c946..6b6e3d2b2 100644
--- a/app/javascript/dashboard/components/widgets/conversation/MessagesView.vue
+++ b/app/javascript/dashboard/components/widgets/conversation/MessagesView.vue
@@ -1,7 +1,7 @@
 <script>
-import { ref, provide } from 'vue';
+import { ref, provide, useTemplateRef } from 'vue';
+import { useElementSize } from '@vueuse/core';
 // composable
-import { useKeyboardEvents } from 'dashboard/composables/useKeyboardEvents';
 import { useLabelSuggestions } from 'dashboard/composables/useLabelSuggestions';
 import { useSnakeCase } from 'dashboard/composables/useTransformKeys';
 
@@ -11,6 +11,7 @@ import MessageList from 'next/message/MessageList.vue';
 import ConversationLabelSuggestion from './conversation/LabelSuggestion.vue';
 import Banner from 'dashboard/components/ui/Banner.vue';
 import Spinner from 'dashboard/components-next/spinner/Spinner.vue';
+import ResizableEditorWrapper from './ResizableEditorWrapper.vue';
 
 // stores and apis
 import { mapGetters } from 'vuex';
@@ -43,21 +44,16 @@ export default {
     Banner,
     ConversationLabelSuggestion,
     Spinner,
+    ResizableEditorWrapper,
   },
   mixins: [inboxMixin],
   setup() {
-    const isPopOutReplyBox = ref(false);
     const conversationPanelRef = ref(null);
-
-    const keyboardEvents = {
-      Escape: {
-        action: () => {
-          isPopOutReplyBox.value = false;
-        },
-      },
-    };
-
-    useKeyboardEvents(keyboardEvents);
+    const resizableEditorWrapperRef = ref(null);
+    const messagesViewRef = useTemplateRef('messagesViewRef');
+    const topBannerRef = useTemplateRef('topBannerRef');
+    const { height: containerHeight } = useElementSize(messagesViewRef);
+    const { height: topBannerHeight } = useElementSize(topBannerRef);
 
     const {
       captainTasksEnabled,
@@ -68,11 +64,15 @@ export default {
     provide('contextMenuElementTarget', conversationPanelRef);
 
     return {
-      isPopOutReplyBox,
       captainTasksEnabled,
       getLabelSuggestions,
       isLabelSuggestionFeatureEnabled,
       conversationPanelRef,
+      resizableEditorWrapperRef,
+      messagesViewRef,
+      topBannerRef,
+      containerHeight,
+      topBannerHeight,
     };
   },
   data() {
@@ -254,6 +254,7 @@ export default {
       this.fetchAllAttachmentsFromCurrentChat();
       this.fetchSuggestions();
       this.messageSentSinceOpened = false;
+      this.resetReplyEditorHeight();
     },
   },
 
@@ -437,26 +438,37 @@ export default {
       const payload = useSnakeCase(message);
       await this.$store.dispatch('sendMessageWithData', payload);
     },
+    toggleReplyEditorSize() {
+      this.resizableEditorWrapperRef?.toggleEditorExpand?.();
+    },
+    resetReplyEditorHeight() {
+      this.resizableEditorWrapperRef?.resetEditorHeight?.();
+    },
   },
 };
 </script>
 
 <template>
-  <div class="flex flex-col justify-between flex-grow h-full min-w-0 m-0">
-    <Banner
-      v-if="!currentChat.can_reply"
-      color-scheme="alert"
-      class="mx-2 mt-2 overflow-hidden rounded-lg"
-      :banner-message="replyWindowBannerMessage"
-      :href-link="replyWindowLink"
-      :href-link-text="replyWindowLinkText"
-    />
-    <Banner
-      v-else-if="hasDuplicateInstagramInbox"
-      color-scheme="alert"
-      class="mx-2 mt-2 overflow-hidden rounded-lg"
-      :banner-message="$t('CONVERSATION.OLD_INSTAGRAM_INBOX_REPLY_BANNER')"
-    />
+  <div
+    ref="messagesViewRef"
+    class="flex flex-col justify-between flex-grow h-full min-w-0 m-0"
+  >
+    <div ref="topBannerRef">
+      <Banner
+        v-if="!currentChat.can_reply"
+        color-scheme="alert"
+        class="mx-2 mt-2 overflow-hidden rounded-lg"
+        :banner-message="replyWindowBannerMessage"
+        :href-link="replyWindowLink"
+        :href-link-text="replyWindowLinkText"
+      />
+      <Banner
+        v-else-if="hasDuplicateInstagramInbox"
+        color-scheme="alert"
+        class="mx-2 mt-2 overflow-hidden rounded-lg"
+        :banner-message="$t('CONVERSATION.OLD_INSTAGRAM_INBOX_REPLY_BANNER')"
+      />
+    </div>
     <MessageList
       ref="conversationPanelRef"
       class="conversation-panel flex-shrink flex-grow basis-px flex flex-col overflow-y-auto relative h-full m-0 pb-4"
@@ -498,13 +510,7 @@ export default {
         />
       </template>
     </MessageList>
-    <div
-      class="flex relative flex-col"
-      :class="{
-        'modal-mask': isPopOutReplyBox,
-        'bg-n-surface-1': !isPopOutReplyBox,
-      }"
-    >
+    <div class="flex relative flex-col bg-n-surface-1">
       <div
         v-if="isAnyoneTyping"
         class="absolute flex items-center w-full h-0 -top-7"
@@ -520,42 +526,12 @@ export default {
           />
         </div>
       </div>
-      <ReplyBox
-        :pop-out-reply-box="isPopOutReplyBox"
-        @update:pop-out-reply-box="isPopOutReplyBox = $event"
-      />
+      <ResizableEditorWrapper
+        ref="resizableEditorWrapperRef"
+        :container-height="Math.max(0, containerHeight - topBannerHeight)"
+      >
+        <ReplyBox @toggle-editor-size="toggleReplyEditorSize" />
+      </ResizableEditorWrapper>
     </div>
   </div>
 </template>
-
-<style scoped lang="scss">
-.modal-mask {
-  @apply fixed;
-
-  &::v-deep {
-    .ProseMirror-woot-style {
-      @apply max-h-[25rem];
-    }
-
-    .reply-box {
-      @apply border border-n-weak max-w-[75rem] w-[70%];
-
-      &.is-private {
-        @apply dark:border-n-amber-3/30 border-n-amber-12/5;
-      }
-    }
-
-    .reply-box .reply-box__top {
-      @apply relative min-h-[27.5rem];
-    }
-
-    .reply-box__top .input {
-      @apply min-h-[27.5rem];
-    }
-
-    .emoji-dialog {
-      @apply absolute ltr:left-auto rtl:right-auto bottom-1;
-    }
-  }
-}
-</style>
diff --git a/app/javascript/dashboard/components/widgets/conversation/ReplyBox.vue b/app/javascript/dashboard/components/widgets/conversation/ReplyBox.vue
index a5122094e..d18be0caa 100644
--- a/app/javascript/dashboard/components/widgets/conversation/ReplyBox.vue
+++ b/app/javascript/dashboard/components/widgets/conversation/ReplyBox.vue
@@ -81,13 +81,7 @@ export default {
     CopilotReplyBottomPanel,
   },
   mixins: [inboxMixin, fileUploadMixin, keyboardEventListenerMixins],
-  props: {
-    popOutReplyBox: {
-      type: Boolean,
-      default: false,
-    },
-  },
-  emits: ['update:popOutReplyBox'],
+  emits: ['toggleEditorSize'],
   setup() {
     const {
       uiSettings,
@@ -797,7 +791,6 @@ export default {
 
         this.clearMessage();
         this.hideEmojiPicker();
-        this.$emit('update:popOutReplyBox', false);
       }
     },
     sendMessageAsMultipleMessages(message, copilotAcceptedMessage = '') {
@@ -1217,8 +1210,9 @@ export default {
         file => !file?.isRecordedAudio
       );
     },
-    togglePopout() {
-      this.$emit('update:popOutReplyBox', !this.popOutReplyBox);
+    toggleEditorSize() {
+      this.$emit('toggleEditorSize');
+      this.$nextTick(() => this.messageEditor?.focusEditorInputField());
     },
     onSubmitCopilotReply() {
       const acceptedMessage = this.copilot.accept();
@@ -1244,9 +1238,8 @@ export default {
       :is-message-length-reaching-threshold="isMessageLengthReachingThreshold"
       :characters-remaining="charactersRemaining"
       :editor-content="message"
-      :popout-reply-box="popOutReplyBox"
       @set-reply-mode="setReplyMode"
-      @toggle-popout="togglePopout"
+      @toggle-editor-size="toggleEditorSize"
       @toggle-copilot="copilot.toggleEditor"
       @execute-copilot-action="executeCopilotAction"
     />
@@ -1275,7 +1268,7 @@ export default {
           v-if="showEmojiPicker"
           v-on-clickaway="hideEmojiPicker"
           :class="{
-            'emoji-dialog--expanded': isOnExpandedLayout || popOutReplyBox,
+            'emoji-dialog--expanded': isOnExpandedLayout,
           }"
           :on-click="addIntoEditor"
         />
@@ -1299,7 +1292,6 @@ export default {
           :show-copilot-editor="copilot.showEditor.value"
           :is-generating-content="copilot.isGenerating.value"
           :generated-content="copilot.generatedContent.value"
-          :is-popout="popOutReplyBox"
           :placeholder="$t('CONVERSATION.FOOTER.COPILOT_MSG_INPUT')"
           @focus="onFocus"
           @blur="onBlur"
diff --git a/app/javascript/dashboard/components/widgets/conversation/ResizableEditorWrapper.vue b/app/javascript/dashboard/components/widgets/conversation/ResizableEditorWrapper.vue
new file mode 100644
index 000000000..4d5c041ac
--- /dev/null
+++ b/app/javascript/dashboard/components/widgets/conversation/ResizableEditorWrapper.vue
@@ -0,0 +1,154 @@
+<script setup>
+import { ref, computed, onMounted, onBeforeUnmount, useTemplateRef } from 'vue';
+import { useEventListener } from '@vueuse/core';
+import { emitter } from 'shared/helpers/mitt';
+import { BUS_EVENTS } from 'shared/constants/busEvents';
+
+const props = defineProps({
+  containerHeight: { type: Number, default: 0 },
+});
+
+const DEFAULT_HEIGHT = 120;
+const MIN_HEIGHT = 80;
+const MIN_MESSAGES_HEIGHT = 200;
+const EXPAND_RATIO = 0.5;
+const RESET_DELAY_MS = 120;
+
+const wrapperRef = useTemplateRef('wrapperRef');
+const surroundingHeight = ref(0);
+const editorHeight = ref(DEFAULT_HEIGHT);
+const isResizing = ref(false);
+const startY = ref(0);
+const startHeight = ref(0);
+let resetTimeoutId = null;
+
+const clamp = (val, min, max) => Math.min(Math.max(val, min), max);
+
+// Measure height of elements surrounding the editor (top panel, email fields, bottom panel)
+const measureSurroundingHeight = () => {
+  if (wrapperRef.value) {
+    surroundingHeight.value = Math.max(
+      0,
+      wrapperRef.value.offsetHeight - editorHeight.value
+    );
+  }
+};
+
+const isContainerReady = computed(() => props.containerHeight > 0);
+
+const sizeBounds = computed(() => {
+  const h = props.containerHeight;
+  const s = surroundingHeight.value;
+  const max = Math.max(MIN_HEIGHT, h - MIN_MESSAGES_HEIGHT - s);
+  const expanded = clamp(Math.floor(h * EXPAND_RATIO - s / 2), MIN_HEIGHT, max);
+  return {
+    min: MIN_HEIGHT,
+    max: isContainerReady.value ? max : DEFAULT_HEIGHT,
+    expanded,
+    default: clamp(DEFAULT_HEIGHT, MIN_HEIGHT, max),
+  };
+});
+
+const clampToBounds = val =>
+  clamp(val, sizeBounds.value.min, sizeBounds.value.max);
+
+const clearDragStyles = () => {
+  Object.assign(document.body.style, { cursor: '', userSelect: '' });
+};
+
+const getClientY = e => (e.touches ? e.touches[0].clientY : e.clientY);
+
+const onResizeStart = event => {
+  editorHeight.value = clampToBounds(editorHeight.value);
+  measureSurroundingHeight();
+  isResizing.value = true;
+  startY.value = getClientY(event);
+  startHeight.value = clampToBounds(editorHeight.value);
+  editorHeight.value = startHeight.value;
+  Object.assign(document.body.style, {
+    cursor: 'row-resize',
+    userSelect: 'none',
+  });
+};
+
+const onResizeMove = event => {
+  if (!isResizing.value) return;
+  if (event.touches) event.preventDefault();
+  editorHeight.value = clampToBounds(
+    startHeight.value + startY.value - getClientY(event)
+  );
+};
+
+const onResizeEnd = () => {
+  if (!isResizing.value) return;
+  isResizing.value = false;
+  clearDragStyles();
+};
+
+const resetEditorHeight = () => {
+  editorHeight.value = sizeBounds.value.default;
+};
+
+const toggleEditorExpand = () => {
+  editorHeight.value = clampToBounds(editorHeight.value);
+  measureSurroundingHeight();
+  const { expanded, max, default: defaultHeight } = sizeBounds.value;
+  const isExpanded = editorHeight.value > defaultHeight;
+  // If expanded is too close to default, use max so the toggle is always noticeable
+  const target = expanded - defaultHeight < 100 ? max : expanded;
+  editorHeight.value = isExpanded ? defaultHeight : target;
+};
+
+const handleMessageSent = () => {
+  clearTimeout(resetTimeoutId);
+  resetTimeoutId = setTimeout(resetEditorHeight, RESET_DELAY_MS);
+};
+
+onMounted(() => {
+  emitter.on(BUS_EVENTS.MESSAGE_SENT, handleMessageSent);
+});
+
+onBeforeUnmount(() => {
+  emitter.off(BUS_EVENTS.MESSAGE_SENT, handleMessageSent);
+  clearTimeout(resetTimeoutId);
+  if (isResizing.value) {
+    isResizing.value = false;
+    clearDragStyles();
+  }
+});
+
+useEventListener(document, 'mousemove', onResizeMove);
+useEventListener(document, 'mouseup', onResizeEnd);
+useEventListener(document, 'touchmove', onResizeMove, { passive: false });
+useEventListener(document, 'touchend', onResizeEnd);
+useEventListener(document, 'touchcancel', onResizeEnd);
+useEventListener(window, 'blur', onResizeEnd);
+
+defineExpose({ toggleEditorExpand, resetEditorHeight });
+</script>
+
+<template>
+  <div
+    ref="wrapperRef"
+    class="relative resizable-editor-wrapper"
+    :style="{
+      '--editor-height': editorHeight + 'px',
+      '--editor-min-allowed': sizeBounds.min + 'px',
+      '--editor-max-allowed': sizeBounds.max + 'px',
+      '--editor-height-transition': isResizing ? 'none' : '180ms ease',
+    }"
+  >
+    <div
+      class="group absolute inset-x-0 -top-4 z-10 flex h-4 cursor-row-resize select-none items-center justify-center bg-gradient-to-b from-transparent from-10% dark:to-n-surface-1/80 to-n-surface-1/90 backdrop-blur-[0.01875rem]"
+      @mousedown="onResizeStart"
+      @touchstart.prevent="onResizeStart"
+      @dblclick="resetEditorHeight"
+    >
+      <div
+        class="w-8 h-0.5 mt-1 rounded-full bg-n-slate-6 group-hover:bg-n-slate-8 transition-all duration-200 motion-safe:group-hover:animate-bounce"
+        :class="{ 'bg-n-slate-8 animate-bounce': isResizing }"
+      />
+    </div>
+    <slot />
+  </div>
+</template>